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Inherited sterility in insects

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Inherited sterility in insects is induced by substerilizing doses of ionizing radiation. When partially sterile males mate with wild females, the radiation-induced deleterious effects are inherited by the F1 generation.[1] As a result, egg hatch is reduced and the resulting offspring are both highly sterile and predominately male. Compared with the high radiation required to achieve full sterility in Lepidoptera, the lower dose of radiation used to induce F1 sterility increases the quality and competitiveness of the released insects as measured by improved dispersal after release, increased mating ability, and superior sperm competition.[2][3][4]

History

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Area-wide integrated pest management programmes using the sterile insect technique (SIT) as a component have been successful against a number of pest flies or Diptera such as the New World screwworm, Cochliomyia hominivorax, various species of tephritidae fruit flies and against tsetse flies (Glossinidae). However, most moths or lepidopterans are more resistant to radiation than dipterans,[5] and as a consequence, the higher dose of radiation required to completely sterilize lepidopterans reduces their performance in the field. One approach to circumvent the negative effects associated with the high radio-resistance of Lepidoptera pests has been the use of inherited sterility or F1 sterility,[6] first documented in studies on the codling moth (Cydia pomonella).[7][8] Inherited sterility has also been documented in the Hemiptera order.

The silk worm Bombyx mori (Lepidoptera: Bombycidae) was the first insect in which inherited sterility was reported.[9] Then inherited sterility was reported in the greater wax moth Galleria mellonella (Lepidoptera:Pyralidae),[10] in the codling moth Cydia pomonella (Lepidoptera: Tortricidae),[8] in the large milkweed bug Oncopeltus fasciatus (Hemiptera: Lygaeidae),[11] in Gonocerus acuteangulatus (Hemiptera: Coreida),[12] in Rhodnius prolixus (Hemiptera: Reduviidae),[13] and in the Two-spotted spider mite Tetranychus urticae (Acari: Tetranychidae).[14]

Genetic basis

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The mechanisms by which mutations cause lethality in Diptera in the developing zygote are well documented.[15][16][17] The primary lesion leading to a dominant lethal mutation is a break in the chromosome, in this case, induced by radiation. When a break is induced in a chromosome in mature sperm, it remains in this condition until after the sperm has entered an egg. Following fusion, nuclear divisions begin, and a break in a chromosome can have drastic effects on the viability of the embryo as development proceeds. During early prophase the broken chromosome undergoes normal replication, but during metaphase the broken ends can fuse leading to the formation of a dicentric chromosome and an acentric fragment. The acentric fragment is frequently lost, while the dicentric fragment forms a bridge at anaphase leading to another chromosomal break. This whole process then repeats itself, leading to the accumulation of serious imbalances in the genetic information of the daughter cells. The accumulation of this genetic damage finally leads to the death of the zygote).

Diptera, Hymenoptera, and Coleoptera orders can be classed as radiation-sensitive, while Lepidoptera, Homoptera and mites (Acari) orders are radiation-resistant.[18] A major difference between these two groups of Insects is that the former group has a localized centromere (monokinetic), while the latter has a diffuse centromere (holokinetic).[19][20][21][22] However, more recent work[23] suggested that lepidopteran chromosomes are intermediate between holokinetic and monocentric chromosomes. In any case, the centromere difference is believed to play a major, although not exclusive, role in radiation sensitivity.[24] It was suggested that possible molecular mechanisms responsible for the high radioresistance in Lepidoptera might include an inducible cell recovery system and a DNA repair probes.[25][26]

Lepidoptera also do not show the classical breakage-fusion-bridge cycle that is a characteristic of dominant lethals induced in Diptera. It appears that lepidopteran chromosomes can tolerate telomere loss without the drastic effects that this has on chromosomes in other orders.[27] Lepidopteran chromosomes possess a localized kinetochore plate to which the spindle microtubules attach during cell division.[28] The kinetochore plates are large and cover a significant portion of the chromosome length, ensuring that more radiation-induced breaks will not lead to the loss of chromosome fragments as is typical in species with monocentric chromosomes. In species with large kinetochore plates, the fragments may persist for a number of mitotic cell divisions, and can even be transmitted through germ cells to the next generation.[29] The plates also reduce the risk of lethality caused by the formation of dicentric chromosomes, acentric fragments, and other unstable aberrations.[27]

Field application

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The F1 sterile progeny produced in the field enhance the efficacy of released partially sterile males, and improve compatibility with other pest control strategies. For example, the presence of F1 sterile progeny can be used to increase the build-up of natural enemies in the field. In addition, F1 sterile progeny can be used to study the potential host and geographical ranges of exotic lepidopteran pests.

Field programmes releasing irradiated moths under an SIT or inherited sterility approach have been in operation since the 1960s. The pink bollworm, Pectinophora gossypiella has been successfully contained since 1969 in cotton areas of the San Joaquin Valley in California and is being successfully targeted for eradication from cotton areas in the south-western USA and north-western Mexico. Since the early 1990s, the codling moth has been successfully suppressed in apple and pear production areas in the Okanagan Valley in British Columbia, Canada, and countries such as Argentina, Brazil and South Africa have plans or programmes against this pest. New Zealand eradicated outbreaks of the Australian painted apple moth, Teia anartoides. Mexico eradicated outbreaks of the cactus moth, Cactoblastis cactorum and the USA contains its advance along the Gulf of Mexico coast.[30][31] South Africa has a programme to suppress the false codling moth, Thaumatotibia leucotreta in citrus orchards.[32] Control of most moth pests is hampered by the increased resistance to the most widely used broad spectrum insecticides; hence the potential for expanded implementation of inherited sterility as part of an area-wide integrated approach is considerable.

See also

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Notes and references

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  1. ^ North, D T (1975). "Inherited Sterility in Lepidoptera". Annual Review of Entomology. 20 (1): 167–182. doi:10.1146/annurev.en.20.010175.001123. ISSN 0066-4170. PMID 1090237.
  2. ^ North, David T.; Holt, Gerald (1968-08-01). "Inherited Sterility in Progeny of Irradiated Male Cabbage Loopers1". Journal of Economic Entomology. 61 (4): 928–931. doi:10.1093/jee/61.4.928. ISSN 1938-291X.
  3. ^ Seth, R.K; Reynolds, S.E (1993). "Induction of inherited sterility in the tobacco hornworm Manduca sexta (Lepidoptera: Sphingidae) by substerilizing doses of ionizing radiation". Bulletin of Entomological Research. 83 (2): 227–235. doi:10.1017/s0007485300034714. ISSN 0007-4853.
  4. ^ Dyck, V. A., editor. Hendrichs, J. (Jorge), editor. Robinson, A. S., editor. (23 February 2006). Sterile insect technique : principles and practice in area wide integrated pest management. Springer. ISBN 978-1-4020-4051-1. OCLC 1154242392. {{cite book}}: |last= has generic name (help)CS1 maint: multiple names: authors list (link)
  5. ^ Bakri, Abdeljelil; Heather, Neil; Hendrichs, Jorge; Ferris, Ian (2005-01-01). "Fifty Years of Radiation Biology in Entomology: Lessons Learned from IDIDAS". Annals of the Entomological Society of America. 98 (1): 1–12. doi:10.1603/0013-8746(2005)098[0001:fyorbi]2.0.co;2. ISSN 0013-8746.
  6. ^ Panel on the Application of Induced Sterility for Control of Lepidopterous Populations (1970 : Vienna, Austria) (1971). Application of induced sterility for control of lepidopterous populations : proceedings. International Atomic Energy Agency. OCLC 1032780537.{{cite book}}: CS1 maint: numeric names: authors list (link)
  7. ^ Proverbs, M. D.; Newton, J. R. (1962-05-01). "Influence of gamma radiation on the development and fertility of the codling moth, Carpocapsa pomonella (l.) (lepidoptera: olethreutidae)". Canadian Journal of Zoology. 40 (3): 401–420. doi:10.1139/z62-038. ISSN 0008-4301.
  8. ^ a b Proverbs, M. D. (1982). "Sterile insect technique in codling moth control". Sterile Insect Technique and Radiation in Insect Control: 85–89.
  9. ^ Astaurov, B. I., and S. L. Frolova . 1935. Artificial mutations in the silkworm (Bombyx mori L.). V. Sterility and spermatogenic anomalies in the progeny of irradiated moths concerning some questions of general biological and mutagenic action of X-rays. Biol. J. 4: 861-894 (in Russian).
  10. ^ Ostriakova-Varshaver, V.P. 1937. The bee moth, Galleria mellonella, as a new object for genetic investigations. II. Cytogenetic analysis of sterility initiated by X-rays in males. [In Russian.] Biologicheskii Zhurnal, 6: 816–836.
  11. ^ LaChance, L. E.; Degrugillier, M. (1969-10-10). "Chromosomal Fragments Transmitted through Three Generations in Oncopeltus (Hemiptera)". Science. 166 (3902): 235–236. Bibcode:1969Sci...166..235L. doi:10.1126/science.166.3902.235. ISSN 0036-8075. PMID 5817763. S2CID 44255849.
  12. ^ Delrio G.;Cavalloro R. 1975. Sterilite hereditaire chez Gonocerus aculteangulatus Goenze (Rhyncote, Coreidea), pp.423-436 In: Sterility principles for insect control. proceedings Symposia, Innsbruck, Austria, 22–26 July 1974. STI/PUB/377. IAEA, Vienna 1975
  13. ^ Maudlin, Ian (1976). "The inheritance of radiation induced semi-sterility in Rhodnius prolixus". Chromosoma. 58 (3): 285–306. doi:10.1007/bf00292095. ISSN 0009-5915. PMID 793795. S2CID 7113515.
  14. ^ Henneberry, T. J. (1964-10-01). "Effects of Gamma Radiation on the Fertility of the Two-Spotted Spider Mite and Its Progeny". Journal of Economic Entomology. 57 (5): 672–674. doi:10.1093/jee/57.5.672. ISSN 1938-291X.
  15. ^ Smith, R. H.; von Borstel, R. C. (1972-12-15). "Genetic Control of Insect Populations: A wide variety of documented genetic methods should be considered for regulation of pest populations". Science. 178 (4066): 1164–1174. doi:10.1126/science.178.4066.1164. ISSN 0036-8075. PMID 4564928.
  16. ^ LaChance, L.E. (1967). "The introduction of dominant lethal mutations by ionizing radiation and chemical as related to sterile-male technique of insect control". In Wright, J. W.; Pal, R.; World Health Organization (eds.). Genetics of insect vectors of disease. pp. 617–650. hdl:10665/38937.
  17. ^ Robinson, A. S. (2005), "Genetic Basis of the Sterile Insect Technique", Sterile Insect Technique, Berlin/Heidelberg: Springer-Verlag, pp. 95–114, doi:10.1007/1-4020-4051-2_4, ISBN 1-4020-4050-4, S2CID 82438765
  18. ^ Bakri, A., K. Mehta, and D. R. Lance. 2005. Sterilizing insects with ionizing radiation. pp. 233-268 In V. A. Dyck, J. Hendrichs, and A. S. Robinson (eds.), Sterile Insect Technique: Principles and Practice in Area-wide Integrated Pest Management. Springer, Dordrecht, The Netherland. 787 pp.
  19. ^ Bauer, Hans (1967). "Die kinetische Organisation der Lepidopteren-Chromosomen". Chromosoma. 22 (2): 101–125. doi:10.1007/bf00326724. ISSN 0009-5915. S2CID 25015956.
  20. ^ LaChance, L. E.; Degrugillier, M. (1969-10-10). "Chromosomal Fragments Transmitted through Three Generations in Oncopeltus (Hemiptera)". Science. 166 (3902): 235–236. Bibcode:1969Sci...166..235L. doi:10.1126/science.166.3902.235. ISSN 0036-8075. PMID 5817763. S2CID 44255849.
  21. ^ Murakami, Akio; Imai, Hirotami T. (1974). "Cytological evidence for holocentric chromosomes of the silkworms, Bombyx mori and B. mandarina, (Bombycidae, Lepidoptera)". Chromosoma. 47 (2): 167–178. doi:10.1007/bf00331804. ISSN 0009-5915. PMID 4141955. S2CID 38442597.
  22. ^ Wrensch, Dana L.; Kethley, John B.; Norton, Roy A. (1994), "Cytogenetics of Holokinetic Chromosomes and Inverted Meiosis: Keys to the Evolutionary Success of Mites, with Generalizations on Eukaryotes", Mites, Boston, MA: Springer US, pp. 282–343, doi:10.1007/978-1-4615-2389-5_11, ISBN 978-1-4613-6012-4
  23. ^ Wolf, Klaus Werner (1996). "The structure of condensed chromosomes in mitosis and meiosis of insects". International Journal of Insect Morphology and Embryology. 25 (1–2): 37–62. doi:10.1016/0020-7322(95)00021-6. ISSN 0020-7322.
  24. ^ Carpenter, J. E.; Bloem, S.; Marec, F. (2005), "Inherited Sterility in Insects", Sterile Insect Technique, Berlin/Heidelberg: Springer-Verlag, pp. 115–146, doi:10.1007/1-4020-4051-2_5, ISBN 1-4020-4050-4, S2CID 85643201
  25. ^ LaChance, Leo E.; Graham, Charles K. (1984). "Insect radiosensitivity: Dose curves and dose-fractionation studies of dominant lethal mutations in the mature sperm of 4 insect species". Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 127 (1): 49–59. doi:10.1016/0027-5107(84)90139-8. ISSN 0027-5107. PMID 6539419.
  26. ^ Koval, Thomas M. (1996). "Moths: Myths and mysteries of stress resistance". BioEssays. 18 (2): 149–156. doi:10.1002/bies.950180211. ISSN 0265-9247. S2CID 86589131.
  27. ^ a b Tothová, Alena; Marec, František (2001-04-01). "Chromosomal principle of radiation-induced F1 sterility in Ephestia kuehniella (Lepidoptera: Pyralidae)". Genome. 44 (2): 172–184. doi:10.1139/g00-107. ISSN 0831-2796. PMID 11341727.
  28. ^ Wolf, Klaus Werner; Novák, Karel; Marec, František (1997). "Kinetic organization of metaphase I bivalents in spermatogenesis of Lepidoptera and Trichoptera species with small chromosome numbers". Heredity. 79 (2): 135–143. doi:10.1038/hdy.1997.136. ISSN 0018-067X. S2CID 34178406.
  29. ^ Marec, František; Tothová, Alena; Sahara, Ken; Traut, Walther (2001). "Meiotic pairing of sex chromosome fragments and its relation to atypical transmission of a sex-linked marker in Ephestia kuehniella (Insecta: Lepidoptera)". Heredity. 87 (6): 659–671. doi:10.1046/j.1365-2540.2001.00958.x. ISSN 0018-067X. PMID 11903561. S2CID 415409.
  30. ^ "Biology, History, Threat, Surveillance and Control of the Cactus Moth, Cactoblastis cactorum, Books & Proceedings, Insect Pest Control - NAFA". www-naweb.iaea.org. Archived from the original on 2020-01-12. Retrieved 2020-08-02.
  31. ^ "Significant damage was avoided to the ecosystem based on prickly pear in Mexico thanks to the eradication of Cactus Moth outbreaks from Caribbean islands of Mexico - Stories, NAFA". www-naweb.iaea.org. Archived from the original on 2020-02-15. Retrieved 2020-08-02.
  32. ^ "ARS Scientists Help Fight Damaging Moth in Africa : USDA ARS". www.ars.usda.gov. Retrieved 2020-08-02.
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