Abstract
The sterile insect technique (SIT) is a method of eradicating insects by releasing mass-reared sterilized males into fields to reduce the hatchability of eggs laid by wild females that have mated with the sterile males. SIT requires mass-production of the target insect, and maintenance of the quality of the mass-reared insects. The most important factor is successful mating between wild females and sterile males because SIT depends on their synchronized copulation. Therefore, understanding the mating systems and fertilization processes of target insects is prerequisite. Insect behavior often has circadian rhythms that are controlled by a biological clock. However, very few studies of relationships between sterile insect quality and circadian rhythm have been performed compared with the amount of research on the mating ability of target insects. The timing of male copulation attempts with receptivity of females is key to successful mating between released males and wild females. Therefore, we should focus on the mechanisms controlling the timing of mating in target insects. On the other hand, in biological control projects, precise timing of the release of natural enemies to attack pest species is required because behavior of pests and control agents are affected by their circadian rhythms. Involving both chronobiologists and applied entomologists might produce novel ideas for sterile insect quality control by synchronized sex between mass-reared and wild flies, and for biological control agent quality by matching timing in activity between predator activity and prey behavior. Control of the biological clocks in sterile insects or biological control agents is required for advanced quality control of rearing insects.
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References
Aigaki T, Fleischmann I, Chen PS, Kubli E (1991) Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron 7:557–563
Alphey LS (2007) Engineering insects for the sterile insect technique. In: Vreysen MJB, Robinson AS, Hendrichs J (eds) Area-wide control of insect pests. Springer, Dordrecht, pp 51–60
Aluja M, Norrbom AL (2000) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC Press, Boca Raton
Arnqvist G, Rowe L (2005) Sexual conflicts. Princeton University Press, Princeton
Bargiello TA, Jackson FR, Young MW (1984) Restoration of circadian behavioural rhythms by gene transfer in Drosophila. Nature 312:752–754
Baumhover AH, Husman CN, Graham AJ (1966) Screw-worm. In: Smith CN (ed) Insect colonization and mass-production. Academic Press, New York, pp 533–554
Birkhead TB, Hosken DJ, Pitnick S (2009) Sperm biology: an evolutionary perspective. Elsevier, Oxford
Bloem KA, Bloem S, Chambers DL (1994) Field assessment of quality: release-recapture of mass-reared Mediterranean fruit flies (Diptera: Tephritidae) of different sizes. Environ Entomol 23:629–633
Boller EF (1972) Behavioural aspects of mass-rearing of insects. Entomophaga 17:9–25
Bush GL, Butlin RK (2004) Sympatric speciation in insects. In: Dickmann U, Doebeli M, Metz JAJ, Tautz D (eds) Adaptive speciation. Cambridge University Press, Cambridge, pp 229–248
Calkins CO (1989) Quality control. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control, vol 3B. Elsevier, Oxford, pp 153–162
Calkins CO, Parker AG (2005) Sterile insect quality. In: Dyck VA, Hendrichs J, Robinson AS (eds) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht, pp 269–296
Calkins CO, Klassen W, Liedo P (1994) Fruit flies and the sterile insect technique. CRC press, Boca Raton
Cayol J (2000) Changes in sexual behavior and life history traits of Tephritid species caused by mass-rearing processes. In: Aluja M, Norrbom AL (eds) Fruit flies (Tephritidae): phylogeny and evolution of behavior. CRC press, Boca Raton, pp 843–860
Chambers DL (1977) Quality control in mass rearing. Annu Rev Entomol 22:289–308
Chapman T, Davies SJ (2004) Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides 25:1477–1490
Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241–244
Chapman T, Miyatake T, Smith H, Partridge L (1998) Interactions of mating, egg production and death rates in Mediterranean fruitfly, Ceratitis capitata females. Proc R Soc Lond B 265:1879–1894
Chen PS, Stumm-Zollinger E, Aigaki T, Balmer J, Bienz M, Bohlen P (1988) A male accessory gland peptide that regulates reproductive behaviour of female D. melanogaster. Cell 54:291–298
Choe JC, Crespi BJ (1997) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge
Cirera S, Aguadè M (1998) The sex peptide gene (ACP 70A) is duplicated in Drosophila subobscura. Gene 210:247–254
Clarke GM, Mckenzie LJ (1992) Fluctuating asymmetry as a quality control indicator for insect mass rearing processes. J Econ Entomol 85:2045–2050
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Sunderland, Massachusetts
Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York
Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature 407:855–856
Davies NB (1991) Mating systems. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach, 3rd edn. Blackwell Scientific Publ, London, pp 263–294
Dodson G (1982) Mating and territoriality in wild Anastrepha suspense (Diptera: Tephritidae) in field cages. J GA Entomol Soc 17:189–200
Dyck VA, Hendrichs J, Robinson AS (2005) Sterile insect technique: principles and practice in area-wide integrated pest management. Springer, Dordrecht
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
Economopoulos AP (1992) Adaptation of the Mediterranean fruit fly (Diptera: Tephritidae) to artificial rearing. J Econ Entomol 85:753–758
Emery P, Stanewsky R, Helfrich-Forster C, Emery-Le M, Hall JC, Rosbash M (2000) Drosophila CRY is a deep brain circadian photoreceptor. Neuron 26:493–504
Emlen DJ, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223
Finney GL, Fisher TW (1964) Culture of entomophagous insects and their hosts. In: DeBach P, Schlinger ET (eds) Biological control of insect pests and weeds. Chapman and Hall, London, pp 328–355
Fuchikawa T, Sanada S, Nishio R, Matsumoto A, Matsuyama T, Yamagishi M, Tomioka K, Tanimura T, Miyatake T (2010) The clock gene Cryptochrome of Bactrocera cucurbitae (Diptera: Tephritidae) in strains with different mating times. Heredity 104:387–392
Fuyama Y (1983) Species-specificity of paragonial substances as an isolating mechanism in Drosophila. Experientia 39:190–192
Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184
Gromko MH, Newport MEA, Kortier MG (1984) Sperm dependence of female receptivity in Drosophila melanogaster. Evolution 38:1273–1282
Harmer AMT, Radhakrishnan P, Taylor PW (2006) Remating inhibition in female Queensland fruit flies: effects and correlated of sperm storage. J Insect Physiol 52:179–186
Hendrichs J, Franz G, Redon P (1995) Increased effectiveness and applicability of the sterile insect technique through male-only release for control of Mediterranean fruit flies during fruiting seasons. J Appl Entomol 119:371–377
Hendrichs J, Robinson AS, Cayol JP, Enkerlin W (2002) Medfly areawide sterile insect technique programs for prevention, suppression or eradication: the importance of mating behavior studies. FL Entomol 85:1–13
Hibino Y, Iwahashi O (1989) Mating receptivity of wild type female for wild type males and mass-reared males in the melon fly, Dacus cucurbitae COQUILLETT (Diptera: Tephritidae). Appl Entomol Zool 24:152–154
Hibino Y, Iwahashi O (1991) Appearance of wild females unreceptive to sterilized males on Okinawa Is. in the eradication program of the melon fly, Dacus cucurbitae COQUILLETT (Diptera: Tephritidae). Appl Entomol Zool 26:265–270
Hill WG (1982) Predictions of response to artificial selection from new mutations. Gen Res 40:255–278
Holland B, Rice WR (1998) Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1–7
Hopper KR, Roush RT, Powell W (1993) Management of genetics of biological-control introductions. Annu Rev Entomol 38:27–51
Huttle MD (1976) Monitoring the quality of laboratory reared insect: a biological and behavioral perspective. Environ Entomol 5:807–814
Iwahashi O, Itô Y, Shiyomi M (1983) A field evaluation of the sexual competitiveness of sterile melon flies, Dacus (Zeugodacus) cucurbitae. Ecol Entomol 8:43–48
Kakinohana H, Yamagishi M (1991) The mass production of the melon fly techniques and problems. In: Kawasaki K, Iwahashi O, Kaneshiro K (eds) Biology and control of fruit flies (Proceedings of the international symposium, Okinawa). Ginowan, Okinawa, Japan, pp 1–10
Knipling EF (1955) Possibilities of insect control or eradication through the use of sexually sterile males. J Econ Entomol 48:459–462
Knipling EF (1964) The potential role of the sterility method for insect population control with special reference to combining this method with conventional methods. USDA-ARS-33-98, pp 1–54
Knipling EF (1979) The basic principles of insect population suppression and management. USDA, Washington DC
Kogan M (1998) Integrated pest management: historical perspective and contemporary developments. Annu Rev Entomol 43:243–270
Konopka RJ, Benzer S (1971) Clock mutants of Drosophila melanogaster. Proc Natl Acad Sci USA 68:2112–2116
Koyama J, Kakinohana H, Miyatake T (2004) Eradication of the melon fly Bactrocera cucurbitae in Japan: Importance of behavior, ecology, genetics, and evolution. Annu Rev Entomol 49:331–349
Kuba H, Itô Y (1993) Remating inhibition in the melon fly, Bactrocera (=Dacus) cucurbitae (Diptera: Tephritidae): copulation with spermless males inhibits female remating. J Ethol 11:23–28
Kuba H, Koyama J (1982) Mating behaviour of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae): comparative studies of one wild and two laboratory strains. Appl Entomol Zool 17:559–568
Kubli E (2003) Sex peptides: seminal peptides of the Drosophila male. Cell Mol Life Sci 60:1689–1704
Kuriwada T, Kumano N, Shiromoto K, Haraguchi D (2010) The effect of mass-rearing on death-feigning behaviour in the sweet potato weevil (Coleoptera: Brentidae). J Appl Entomol 134:652–658
Leahy MG (1967) Nonspecificity of the male factor enhancing egg-laying in Diptera. J Insect Physiol 13:1283–1292
Leahy MG, Craig GB (1965) Accessory gland substance as a stimulant for oviposition in Aedes aegypti and A. albopictus. Mosquito News 25:448–452
Leppla NC (1989) Laboratory colonization of fruit flies. In: Robinson AS, Hooper G (eds) Fruit flies: their biology, natural enemies and control Vol. 3B. Elsevier, Oxford, pp 91–103
Letsinger JT, Gromko MH (1985) Role of sperm numbers in sperm competition and female remating in Drosophila melanogaster. Genetica 66:195–202
Loukas M, Economopoulos AP, Zouros E, Vergini Y (1985) Genetic changes in artificially reared colonies of the Olive fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 78:159–165
Mackauer M (1972) Genetic aspects of insect production. Entomophaga 17:27–48
Mackauer M (1976) Genetic problems in the production of biological control agents. Annu Rev Entomol 21:369–385
Manning A (1962) A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature 194:252–253
Manning A (1967) The control of sexual receptivity in female Drosophila. Anim Behav 15:239–250
Matsumoto A, Ukai-Tadenuma M, Yamada RG, Houl J, Uno KD, Kasukawa T, Dauwalder B, Itoh TQ, Takahashi K, Ueda R, Hardin PE, Tanimura T, Ueda HR (2007) A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. Genes Dev 21:1687–1700
Matsumoto A, Ohta Y, Itoh TQ, Sanada-Morimura S, Matsuyama T, Fuchikawa T, Tanimura T, Miyatake T (2008) Period gene of Bactrocera cucurbitae (Diptera: Tephritidae) among strains with different mating times and sterile insect technique. Ann Entomol Soc Am 101:1121–1130
Matsuyama T, Kuba H (2009) Mating time and call frequency of males between mass-reared and wild strains of melon fly, Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Appl Entomol Zool 44:309–314
Mayr E (1954) Change of genetic environment and evolution. In: Huxley J, Hardy AC, Ford EB (eds) Evolution as a process. Macmillan, New York, pp 157–180
Miyatake T (1995) Two-way artificial selection for developmental period in Bactrocera cucurbitae (Diptera: Tephritidae). Ann Entomol Soc Am 88:848–855
Miyatake T (1997a) Genetic trade-off between early fecundity and longevity in Bactrocera cucurbitae (Diptera: Tephritidae). Heredity 78:93–100
Miyatake T (1997b) Correlated responses to selection for developmental period in Bactrocera cucurbitae (Diptera: Tephritidae): time of mating and daily activity rhythms. Behav Genet 27:489–498
Miyatake T (1998) Genetic changes of life history and behavioral traits during mass-rearing in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Res Popul Ecol 40:301–310
Miyatake T (2002) Circadian rhythm and time of mating in Bactrocera cucurbitae (Diptera: Tephritidae) selected for age at reproduction. Heredity 88:302–306
Miyatake T, Shimizu T (1999) Genetic correlations between life-history and behavioral traits can cause reproductive isolation. Evolution 53:201–208
Miyatake T, Yamagishi M (1993) Active quality control in mass reared melon flies: quantitative genetic aspects. In: EA IA (ed) Management of insect pests: nuclear and related molecular and genetic techniques. IAEA, Vienna, pp 201–213
Miyatake T, Yamagishi M (1999) Rapid evolution of larval development time during mass-rearing in the melon fly, Bactrocera cucurbitae. Res Popul Ecol 41:291–297
Miyatake T, Chapman T, Partridge L (1999) Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. J Insect Physiol 45:1021–1028
Miyatake T, Matsumoto A, Matsuyama T, Ueda HR, Toyosato T, Tanimura T (2002) The period gene and allochronic reproductive isolation in Bactrocera cucurbitae. Proc R Soc B 269:2467–2472
Mossinson S, Yuval B (2003) Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. J Insect Physiol 49:561–567
Nakayama S, Seko T, Takatsuki J, Miura K, Miyatake T (2010) Walking activity of flightless Harmonia axyridis (Coleoptera: Coccinellidae) as a biological control agent. J Econ Entomol 103:1564–1568
Ochieng’-Odero JPR (1994) Does adaptation occur in insect rearing systems, or is it a case of selection, acclimatization and domestication? Insect Sci Appl 15:1–7
Opender K, Gerrit WC, Norman E (2008) Areawide pest management: theory and implementation. CAB International, Oxford
Orozco D, Lopez RO (1993) Mating competitiveness of wild and laboratory mass-reared medflies: effect of male size. In: Aluja M, Liedo P (eds) Fruit flies: biology and management. Springer, New York, pp 185–188
Radharkrishnan P, Taylor PW (2007) Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies. J Insect Physiol 53:741–745
Ramalingam S, Craig GBJ (1976) Functions of the male accessory gland secretions of Aedes mosquitos (Diptera: Culicidae): transplantation studies. Can Entomol 108:955–960
Rauston JR, Graham HM, Lingren PD, Snow JW (1976) Mating interaction of native and laboratory-reared tobacco budworms released in the field. Environ Entomol 5:195–198
Reisen WK, Sakai RK, Rathor RH, Rana K, Azza K, Niaz S (1980) Field competitiveness of Culex tritaeniorhynchus Giles males carrying a complex chromosomal aberration: a second experiment. Ann Entomol Soc Am 73:479–484
Robacker DC, Hart WG (1985) Courtship and territoriality of laboratory-reared Mexican fruit flies, Anastrepha ludens (Diptera: Tephritidae), in cages containing host and nonhost trees. Ann Entomol Soc Am 78:488–494
Robacker DC, Mangan RL, Moreno DS, Tarshis Moreno AM (1991) Mating behavior and male mating success in wild Anastrepha ludens (Diptera: Tephritidae) on a field-caged host tree. J Insect Behav 4:471–487
Rönn J, Katvala M, Arnqvist G (2007) Coevolution between harmful male genitalia and female resistance in seed beetles. Proc Natl Acad Sci USA 104:10921–10925
Rössler Y (1975) Reproductive differences between laboratory-reared and field-collected populations of the Mediterranean fruitfly, Ceratitis capitata. Ann Entomol Soc Am 68:987–991
Sakai T, Ishida N (2001) Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci USA 98:9221–9225
Schmidt T, Choffat Y, Klauser S, Kubli E (1993) The Drosophila melanogaster sex peptide: a molecular analysis of structure function relationships. J Insect Physiol 39:361–368
Sehgal A, Price JL, Man B, Young MW (1994) Loss of circadian behavioral rhythms and per RNA oscillations in the Drosophila mutant timeless. Science 263:1603–1606
Sharp JL, Boller EF, Chambers DL (1983) Selection for flight propensity of laboratory and wild strains of Anastrepha suspense and Ceratitis capitata (Diptera: Tephritidae). J Econ Entomol 76:302–305
Shelly TE (2000) Flower-feeding affects mating performance in male oriental fruit fly Bactrocera dorsalis. Ecol Entomol 25:109–114
Shelly TE (2001) Exposure to α-copaene and α-copaene-containing oils enhances mating success of male Mediterranean fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 94:497–502
Shelly T (2010) Effects of methyl eugenol and raspberry ketone/cue lure on the sexual behavior of Bactrocera species (Diptera: Tephritidae). Appl Entomol Zool 45:349–361
Shelly TE, Whittier TS (1997) Lek behavior of insects. In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge
Shelly T, Dang C, Kennelly S (2004) Exposure to orange (Citrus sinensis L.) trees, fruit, and oil enhances mating success of male Mediterranean fruit flies (Ceratitis capitata [Wiedemann]). J Insect Behav 17:303–315
Shimizu T, Miyatake T, Watari Y, Arai T (1997) A gene pleiotropically controlling developmental and circadian periods in the melon fly, Bactrocera cucurbitae (Diptera: Tephritidae). Heredity 79:600–605
Shimoji Y, Miyatake T (2002) Adaptation to artificial rearing during successive generations in the West Indian sweetpotato weevil, Euscepes postfasciatus (Coleoptera: Curuculionidae). Ann Entomol Soc Am 95:735–739
Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton
Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton
Simmons GS, Suckling DM, Carpenter JE, Addison MF, Dyck VA, Vresen MJB (2010) Improved quality management to enhance the efficacy of the sterile insect technique for lepidopteran pests. J Appl Entomol 134:261–273
Smith RL (1984) Sperm competition and the evolution of animal mating systems. Academic Press, New York
Soemori H (1980) Difference in mating occurrence between mass-reared and wild strains of the melon fly, Dacus cucurbitae COQUILLETT. Bull Okinawa Pref Agric Exp Stn 5:69–71
Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC (1998) The cry b mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95:681–692
Suenaga H, Kamiwada H, Tanaka A, Chishaki N (1992) Difference in the timing of larval jumping behavior of mass-reared and newly-colonized strains of the melon fly, Dacus cucurbitae (Diptera: Tephritidae). Appl Entomol Zool 27:177–183
Suenaga H, Tanaka A, Kamiwada H, Kamikado T, Chishaki N (2000) Long-term changes in age-specific egg production of two Bactrocera cucurbitae (Diptera: Tephritidae) strains mass-reared under different selection regimes, with different egg collection methods. Appl Entomol Zool 35:13–20
Suzuki Y, Koyama J (1980) Temporal aspects of mating behavior of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae): a comparison between laboratory and wild strains. Appl Entomol Zool 15:215–224
Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, Cambridge
Ueda H, Matsumoto A, Kawamura M, Iino M, Tanimura T, Hashimoto S (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem 277:14048–14052
Van Driesche RG, Bellows TSB Jr (1997) Biological control. Kluwer Academic Publ, Dordrecht
Van Lenteren JC (2003) Quality control and production of biological control agents: theory and testing procedures. CABI Publication, Oxon
Van Valen L (1962) A study of fluctuating asymmetry. Evolution 16:125–142
Vargas RI, Carey JR (1989) Comparison of demographic parameters for wild and laboratory-adapted Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 82:55–59
Vera MT, Wood RJ, Cladera JL, Gilburn AS (2002) Factors affecting female remating frequency in the Mediterranean fruit fly (Diptera: Tephritidae). Fl Entomol 85:156–164
Vreysen MJB, Robinson AS, Hendrichs J (2007) Area-wide control of insect pests: from research to field implementation. Springer, Dordrecht, The Netherlands
Wajnberg E (1991) Quality control of mass-reared arthropods: a genetical and statistical approach. In: Proceedings of the 5th workshop of the global IOBC working group “Quality Control of Mass Reared Organisms”. Wageningen, pp 15–25
Wajnberg E (2003) Measuring genetic variation in natural enemies used for biological control: why and how? In: Ehler LE, Sforza R, Mateille T (eds) Genetics, evolution and biological control. CABI Publishing, Wallingford, UK
Westneat DF, Fox CW (2010) Evolutionary behavioral ecology. Oxford University Press, Oxford
Wolfner MF (1997) Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem Mol Biol 27:179–192
Wong TTY, Nakahara LM (1978) Sexual development and mating response of laboratory-reared and native Mediterranean fruit flies. Ann Entomol Soc Am 71:592–596
Wong TTY, Couey HM, Nishimoto JI (1982) Oriental fruit fly: sexual development and mating response of laboratory-reared and wild flies. Ann Entomol Soc Am 75:191–194
Yamane T, Miyatake T (2010) Induction of oviposition by injection of male-derived extracts in two Callosobruchus species. J Insect Physiol 56:1783–1788
Yamane T, Miyatake T, Kimura Y (2008) Female mating receptivity after injection of male-derived extracts in Callosobruchus maculatus. J Insect Physiol 541:1522–1527
Zervas GA, Economopoulos AP (1982) Mating frequency in caged populations of wild and artificially reared (normal or gamma-sterilized) olive fruit flies. Environ Entomol 11:17–20
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The author was invited to write this report as the prize review of the Society for Japanese Applied Entomology and Zoology. I thank the Society and all colleagues, especially entomologists in Okinawa prefecture and Okayama University, for their support of this study. The study was supported by Plant Breeding and Environmental Research Project Entrusting to Prefectural Institutes; Agriculture, Forestry and Fisheries Research Council (Ministry of Agriculture, Forestry and Fisheries), Japan.
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This review was invited to write as the Price Award of the Japanese Society of Applied Entomology and Zoology.
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Miyatake, T. Insect quality control: synchronized sex, mating system, and biological rhythm. Appl Entomol Zool 46, 3–14 (2011). https://doi.org/10.1007/s13355-010-0017-7
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DOI: https://doi.org/10.1007/s13355-010-0017-7