Eur. J. Entomol. 119: 300-308, 2022 | DOI: 10.14411/eje.2022.031

The association of the development of the internal reproductive organs of male desert locusts, Schistocerca gregaria (Orthoptera: Acrididae), with age, phase and the effect of exposure to pheromonesOriginal article

Satoshi HIROYOSHI1, 2, Takayuki MITSUNAGA3, Gadi V.P. REDDY4
1 Department of Chemical Ecology, International Centre of Insect Physiology and Ecology (I.C.I.P.E.), Nairobi, P.O. Box 30772, Kenya
2 Kawagoe, Saitama 350-1115, Japan; e-mail: satoshi_hiroyoshi@yahoo.co.jp
3 Institute for Plant Protection, National Agriculture and Food Research Organization, 2-1-18 Kannondai, Tsukuba, Ibaraki 305-8602, Japan; e-mail: aeiou@affrc.go.jp
4 USDA-ARS, Southern Insect Management Research Unit, 141 Experiment Station Road, P.O. Box 346, Stoneville, MS 38776, U.S.A.; e-mail: gadi.reddy@usda.gov

The regulation of the development of the male reproductive organs in insects is still an open question. Although the desert locust, Schistocerca gregaria, has been extensively examined, there is little information on the effects of phase and pheromones on the development of the male reproductive organs. This study clarified the association of these two factors with reproductive development (length or width of each organ) of the testis, testicular follicles, accessory glands, and seminal vesicles in this locust. The width of the follicles and width and length of the accessory gland mass are significantly associated with phase (solitary or gregarious). Developmen of all reproductive organs is age dependent as these organs developed in the adult stage. The development of follicles and accessory glands (width) in males in the first two weeks of adulthood was promoted by exposing them to pheromones from mature adults, but not from nymphs. These results indicate the incidence of male reproductive development is associated with phase and affected by pheromones.

Keywords: Accessory gland, reproduction, seminal vesicle, sperm, testis

Received: March 11, 2022; Revised: July 12, 2022; Accepted: July 12, 2022; Published online: August 11, 2022  Show citation

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HIROYOSHI, S., MITSUNAGA, T., & REDDY, G.V.P. (2022). The association of the development of the internal reproductive organs of male desert locusts, Schistocerca gregaria (Orthoptera: Acrididae), with age, phase and the effect of exposure to pheromones. EJE, 119, Article 300-308. https://doi.org/10.14411/eje.2022.031
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    References

    1. Amerasinghe F.P. 1978a: Pheromonal effects on sexual maturation, yellowing, and the vibration reaction in immature male desert locusts (Schistocerca gregaria). - J. Insect Physiol. 24: 309-314. Go to original source...
    2. Amerasinghe F.P. 1978b: Effects of JH I and JH II on yellowing, sexual activity and pheromone production in allatectomized male Schistocerca gregaria. - J. Insect Physiol. 24: 603-611. Go to original source...
    3. Ascerno M.E., Hower Jr, A.A. & Smilowitz Z. 1978: Gonadal development of laboratory-reared male alfalfa weevils, Hypera postica. - Ann. Entomol. Soc. Am. 71: 239-242. Go to original source...
    4. Assad Y.O.H., Hassanali A., Torto B., Mahamat H., Bashir N.H.H. & Bashir S.E. 1997: Effects of fifth-instar volatiles on sexual maturation of adult desert locust Schistocerca gregaria. - J. Chem. Ecol. 23: 1377-1388. Go to original source...
    5. Avruch L.I. & Tobe S.S. 1978: Juvenile hormone biosynthesis by the corpora allata of the male desert locust, Schistocerca gregaria, during sexual maturation. - Can. J. Zool. 56: 2097-2102. Go to original source...
    6. Bakr R.F.A., Mohammed M.I., Elazeem A., El-Gammal M. & Mahdy N.M. 2010: Histopathological change in the testis of the desert locust Schistocerca gregaria (Forskal) induced by the IGR Consult and Lufox. - Egypt. Acad. J. Biol. Sci. 1: 23-28. Go to original source...
    7. Boerjan B., Tobback J., Vandersmissen H.P., Huybrechts R. & Schoofs L. 2012: Fruitless RNAi knockdown in the desert locust, Schistocerca gregaria, influences male fertility. - J. Insect Physiol. 58: 265-269. Go to original source...
    8. Breuer M., Hoste B. & de Loof A. 2003: The endocrine control of phase transition: some new aspects. - Physiol. Entomol. 28: 3-10. Go to original source...
    9. Buhl J., Sumpter D.J.T., Couzin I.D., Hale J.J., Despland E., Miller E.R. & Simpson S.J. 2006: From disorder to order in marching locusts. - Science 312: 1402-1406. Go to original source...
    10. Cantacuzène A.M., Lauverjat S. & Papillon M. 1972: Influence de la température d'élevage sur les caractères histologiques de l'appareil génital de Schistocerca gregaria. - J. Insect Phy­siol. 18: 2077-2093. Go to original source...
    11. Chase J.A. & Gilliland Jr, F.R. 1972: Testicular development in the tobacco budworm. - Ann. Entomol. Soc. Am. 65: 901-906. Go to original source...
    12. Chaudhury M.F.B. & Raun E.S. 1966: Spermiogenesis and testicular development of the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyraustidae). - Ann. Entomol. Soc. Am. 59: 1157-1159. Go to original source...
    13. Claeys I., Simonet G., Breugelmans B., van Soest S., Franssens V., Sas F., de Loof A. & Broeck J.V. 2005: Quantitative real-time RT-PCR analysis in desert locusts reveals phase dependent differences in neuroparsin transcript levels. - Insect Mol. Biol. 14: 415-422. Go to original source...
    14. Coggins P.B. 1973: The effect of X-radiation on spermatogenesis and the fertility of Schistocerca gregaria (Forsk.). - J. Embryol. Exp. Morph. 30: 163-177. Go to original source...
    15. Couche G.A. & Gillott C. 1987: Development of secretory activity in the long hyaline gland of the male migratory grasshopper, Melanoplus sanguinipes (Fabr.) (Orthoptera: Acrididae). - Int. J. Insect Morphol. Embryol. 16: 355-367. Go to original source...
    16. Das N.K., Siegel E.P. & Alfert M. 1965: Synthetic activities during spermatogenesis in the locust. - J. Cell Biol. 25: 387-395. Go to original source...
    17. Dhadialla T.S., Odhiambo T.R. & Wagner G.G. 1986: Immunochemical ablation of accessory reproductive glands of the male desert locust. - Insect Sci. Appl. 7: 465-470. Go to original source...
    18. Dirsh V.M. 1951: A new biometrical phase character in locusts. - Nature 167: 281-282. Go to original source...
    19. Dushimirimana S., Hance T. & Damiens D. 2012: Comparison of reproductive traits of regular and irradiated male desert locust Schistocerca gregaria (Orthoptera: Acrididae): Evidence of last-male sperm precedence. - Biol. Open 1: 232-236. Go to original source...
    20. Ellis P.E., Carlisle D.B. & Osborne D.J. 1965: Desert locusts: sexual maturation delayed by feeding on senescent vegetation. - Science 149: 546-547. Go to original source...
    21. Ernst U.R., van Hiel M.B., Depuydt G., Boerjan B., de Loof A. & Schoofs L. 2015: Epigenetics and locust life phase transitions. - J. Exp. Biol. 218: 88-99. Go to original source...
    22. Ferenz H.-J. & Seidelmann K. 2003: Pheromones in relation to aggregation and reproduction in desert locusts. - Physiol. Entomol. 28: 11-18. Go to original source...
    23. Gillott C. & Venkatesh K. 1985: Accumulation of secretory proteins in the accessory reproductive glands of the male migratory grasshopper, Melanoplus sanguinipes: a developmental study. - J. Insect Physiol. 31: 195-204. Go to original source...
    24. Golov Y., Rillich J., Harari A. & Ayali A. 2018: Precopulatory behavior and sexual conflict in the desert locust. - Peer J. 6: e44356, 24 pp. Go to original source...
    25. Hamilton A.G. 1936: The relation of humidity and temperature to the development of three species of African locusts - Locusta migratoria migratorioides (R. & F.), Schistocerca gregaria (Forsk.), Nomadacris septemfasciata (Serv.). - Trans. R. Entomol. Soc. Lond. 85: 1-60. Go to original source...
    26. Hassanali A., Njagi P.G.N. & Bashir M.O. 2005: Chemical ecology of locusts and related Acridids. - Annu. Rev. Entomol. 50: 223-245. Go to original source...
    27. Hiroyoshi S. 2000: Effects of aging, temperature and photoperiod on testis development of Polygonia c-aureum (Lepidoptera: Nymphalidae). - Entomol. Sci. 3: 227-236.
    28. Hiroyoshi S. & Moriya S. 1999: Effects of aging and temperature on the male's reproductive development of the West Indian sweetpotato weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae). - Entomol. Sci. 2: 165-171.
    29. Hiroyoshi S., Kohama T. & Reddy G.V.P. 2016: Age-related sperm production, transfer, and storage in the sweet potato weevil, Cylas formicarius (Fabricius) (Coleoptera: Curculionidae). - J. Insect Behav. 29: 689-707. Go to original source...
    30. Hiroyoshi S., Mitsunaga T., Ganaha-Kikumura T. & Reddy G.V.P. 2021a: Effects of age, phase variation and pheromones on male sperm storage in the desert locust, Schistocerca gregaria. - Insects 12: 642, 21 pp. Go to original source...
    31. Hiroyoshi S., Mitsunaga T. & Reddy G.V.P. 2021b: Effects of temperature, age and stage on testis development in diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). - Physiol. Entomol. 46: 200-209. Go to original source...
    32. Hoque M.R. 1992: Comparative morphology of the reproductive systems of Heliothis armigera (Hubner) and Heliothis punctigera Wallengren (Lepidoptera: Noctuidae). - Bangladesh J. Zool. 20: 17-26.
    33. Ignell R., Couillaud F. & Anton S. 2001: Juvenile-hormone-mediated plasticity of aggregation behaviour and olfactory processing in adult desert locusts. - J. Exp. Biol. 204: 249-256. Go to original source...
    34. Inayatullah C., Bashir S.E. & Hassanali A. 1994: Sexual behavior communication in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae): Sex pheromone in solitaria. - Environ. Entomol. 23: 1544-1551. Go to original source...
    35. Jones R.T. 1978: The blood-germ cell barrier in male Shistocerca gregaria: The time of its establishment and factors affecting its formation. - J. Cell Sci. 31: 145-163. Go to original source...
    36. Kotaki T. & Yagi S. 1989: Hormonal control of adult diapause in the brown-winged green bug, Plautia stali Scott (Heteroptera: Pentatomidae). - Appl. Entomol. Zool. 24: 42-51. Go to original source...
    37. Loher W. 1960: The chemical acceleration of the maturation process and hormonal control in the male of the desert locust. - Proc. R. Soc. Lond. (B) 153: 380-397. Go to original source...
    38. Maeno K. & Tanaka S. 2011: Phase-specific responses to different qualities of food in the desert locust, Schistocerca gregaria: Developmental, morphological and reproductive characteristics. - J. Insect Physiol. 57: 514-520. Go to original source...
    39. Nilakhe S. & Earle N. 1976: Sperm production in normal vs. sterile boll weevils. - J. Econ. Entomol. 69: 609-613. Go to original source...
    40. Norris M.J. 1952: Reproduction in the desert locust (Schistocerca gregaria Forsk.) in relation to density and phase. - Anti-Locust Bull. 13: 1-49.
    41. Norris M.J. 1954: Sexual maturation in the desert locust (Schistocerca gregaria Forsk.) with special reference to the effects of grouping. - Anti-Locust Bull. 18: 1-44.
    42. Norris M.J. 1964: Accelerating and inhibiting effects of crowding on sexual maturation in two species of locusts. - Nature 203: 784-785. Go to original source...
    43. Norris M.J. & Pener M.P. 1965: An inhibitory effect of allatectomized males and females on the sexual maturation of young male adults of Schistocerca gregaria (Forsk.) (Orthoptera: Acrididae). - Nature 204: 1122. Go to original source...
    44. Odhiambo T.R. 1969: The architecture of the accessory reproductive glands of the desert locust IV Fine structure of the glandular epithelium. - Trans. R. Soc. Lond. (B) 256: 85-114. Go to original source...
    45. Odhiambo T.R. 1970: The architecture of the accessory reproductive glands of the male desert locust. - Tissue & Cell 2: 233-248. Go to original source...
    46. Omura S. 1936: Studies on the reproductive system of the male of Bombyx mori I. Structure of the testis and the intratesticular behavior of the spermatozoa - J. Facul. Agr. Hokkaido Imp. Univ. Sapporo 38: 151-181.
    47. Pener M.P. 1967: Effects of allatectomy and sectioning of the nerves of the corpora allata on oöcyte growth, male sexual behaviour, and colour change in adults of Schistocerca gregaria. - J. Insect Physiol. 13: 665-684. Go to original source...
    48. Pener M.P. 1991: Locust phase polymorphism and its endocrine relations. - Adv. Insect Physiol. 23: 1-79. Go to original source...
    49. Pener M.P. & Simpson S.J. 2009: Locust phase polymorphism: an update. - Adv. Insect Physiol. 36: 1-272. Go to original source...
    50. Pickford R. & Gillott C. 1971: Insemination in the migratory grasshopper, Melanoplus sanguinipes (Fabr). - Can. J. Zool. 49: 1583-1588. Go to original source...
    51. Pickford R. & Gillott C. 1972: Coupling behaviour of the migratory grasshopper, Melanoplus sanguinipes (Orthoptera: Acrididae). - Can. Entomol. 104: 873-879. Go to original source...
    52. Pickford R. & Padgham D.E. 1973: Spermatophore formation and sperm transfer in the desert locust, Schistocerca gregaria (Orthoptera: Acrididae). - Can. Entomol. 105: 613-618. Go to original source...
    53. Rai M.M., Hassanali A., Saini R.K., Odongo H. & Kahoro H. 1997: Identification of components of the oviposition aggregation pheromone of the gregarious desert locust, Schistocerca gregaria (Forskal). - J. Insect Physiol. 43: 83-87. Go to original source...
    54. Richard M.J. & El-Mangoury M.A. 1968: Further experiments on the effects of social factors on the rate of sexual maturation in the desert locust. - Nature 219: 865-866. Go to original source...
    55. Scheppens M.H.M. & Wysoki M. 1985: Testicular development, spermatogenesis and chromosomes of Boarmia selenaria Schiff. (Lepidoptera: Geometridae). - Int. J. Invert. Reprod. Dev. 8: 337-348. Go to original source...
    56. Seidelmann K. & Ferenz H.-J. 2002: Courtship inhibition pheromone in desert locusts, Schistocerca gregaria. - J. Insect Physiol. 48: 991-996. Go to original source...
    57. Simpson S.J.& Miller G.A. 2007: Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: a review of current understanding. - J. Insect Physiol. 53: 869-876. Go to original source...
    58. Sugawara R. & Tanaka S. 2018: Environmental and hormonal control of body color polyphenism in late-instar desert locust nymphs: Role of the yellow protein. - Insect Biochem. Mol. Biol. 93: 27-36. Go to original source...
    59. Sugawara R., Tanaka S., Jouraku A. & Shiotsuki T. 2018: Identification of a transcription factor that functions downstream of corazonin in the control of desert locust gregarious body coloration. - Insect Biochem. Mol. Biol. 97: 10-18. Go to original source...
    60. Szöllösi A. 1982: Relationships between germ and somatic cells in the testes of locusts and moths. In King R.C. & Akai H. (eds): Insect Ultrastructure. Vol. 1. Plenum Press, New York, pp. 32-63. Go to original source...
    61. Tanaka S. 2005: Hormonal control of phase polyphenism in locusts. - Formosan. Entomol. 25: 131-143.
    62. Tanaka S. & Nishide Y. 2012: Do desert locust hoppers develop gregarious characteristics by watching video? - J. Insect Physiol. 58: 1060-1071. Go to original source...
    63. Tawfik A.I., Osir E.O., Hassanali A. & Ismail S.H. 1997: Effects of juvenile hormone treatment on phase changes and pheromone production in the desert locust, Schistocerca gregaria (Forskal) (Orthoptera: Acrididae). - J. Insect Physiol. 43: 1177-1182. Go to original source...
    64. Tawfik A.I., Treiblmayr K., Hassanali A. & Osir E.O. 2000: Time-course haemolymph juvenile hormone titres in solitarious and gregarious adults of Schistocerca gregaria, and their relation to pheromone emission, CA volumetric changes and oocyte growth. - J. Insect Physiol. 46: 1143-1150. Go to original source...
    65. Tobback J., Boerjan B., Vandersmissen H.P. & Huybrechts R. 2011: The circadian clock genes affect reproductive capacity in the desert locust Schistocerca gregaria. - Insect Biochem. Mol. Biol. 41: 313-321. Go to original source...
    66. van Lommel J., Lenaerts C., Delgouffe C. & vanden Broeck J. 2022: Knockdown of ecdysone receptor in male desert locusts affects relative weight of accessory glands and mating behavior. - J. Insect Physiol. 138: 104368, 11 pp. Go to original source...
    67. van Wielendaele P., Wynant N., Dillen S., Zels S., Badisco L. & Broeck J.V. 2013: Neuropeptide F regulates male reproductive processes in the desert locust, Schistocerca gregaria. - Insect Biochem. Mol. Biol. 43: 252-259. Go to original source...
    68. Ward P.I. & Simmons L.W. 1991: Copula duration and testes size in the yellow dung fly, Scathophaga stercoraria (L.): the effects of diet, body size, and mating history. - Behav. Ecol. Sociobiol. 29: 77-85. Go to original source...

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