Influence of remating on sterile insect technique in Ceratitis capitata (Diptera: Tephritidae): a molecular approach

Authors

DOI:

https://doi.org/10.1590/1983-21252023v36n308rc

Keywords:

Genetic markers. Fruitgrowing. Mass rearing. Medfly. Spermathecae.

Abstract

The Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), is one of the most harmful species to world horticulture, thus requiring suppression or eradication programs. The sterile insect technique is widely used for autocidal control of nuisance insects because it neither releases exotic agents into the environment nor introduces new genetic material into existing populations. In 2005, the Moscamed Brasil biofactory imported the tsl Vienna 8 C. capitata strain from the International Atomic Energy Agency (IAEA); this action required genetic testing of the strain’s biological characteristics. The objective of this study was to discriminate males of wild populations from tsl Vienna 8 using molecular markers, and to conclude which male line dominated in a remating condition. Four crosses, each using 100 males and 100 females, were performed: wild female × wild male; wild female × tsl Vienna 8 male; wild female × wild male, followed by remating with tsl Vienna 8 males after 48 h, and wild female × tsl Vienna 8 male, followed by remating with wild males after 48 h. The results showed that the tsl Vienna 8 strain is compatible with wild females from the São Francisco Valley region and that these males can successfully transfer their sperm to the female spermathecae. Regarding remating, the sperm of the second male dominated over that of the first one. Based on these findings, the sterile insect technique success may be reduced, since the progeny of a female that remates with a wild male could be viable.

Downloads

Download data is not yet available.

References

AQUINO, J. C.; JOACHIM-BRAVO, I. S. Relevance of male size to female mate choice in Ceratitis capitata (Diptera: Tephritidae): investigations with wild and laboratory-reared flies. Journal of Insect Behavior, 27: 162-176, 2013.

ANJOS-DUARTE, C. S.; COSTA, A. M.; JOACHIM-BRAVO, I. S. Influence of female age on variation of mate choice behavior in Mediterranean fruit fly (Diptera: Tephritidae). Journal of Insect Behavior, 24: 11-21, 2011.

ARAUJO, E. L.; ZUCCHI, R. A. Moscas-das-frutas (Diptera: Tephritidae) em goiaba (Psidium guajava L.), em Mossoró, RN. Arquivos do Instituto Biológico,70: 73-77, 2003.

BONIZZONI, M. et al. Microsatellite analysis reveals remating by wild Mediterranean fruit fly females, Ceratitis capitata. Molecular Ecology, 11: 1915-1921, 2002.

BONIZZONI, M. et al. Is polyandry a common event among wild populations of the pest Ceratitis capitata? Journal of Economic Entomology, 99: 1420-1429, 2006.

BLOEM, K. et al. Female Medfly refractory period: effect of male reproductive status. In: ALUJA, M.; LIEDO, P. (Eds.). Fruit Flies: Biology and Management. New York, USA: Springer, 1993. v. 1, cap. 35, p. 189-190.

BRICEÑO, D.; EBERHARD, W.; SHELLY, T. Male courtship behavior in Ceratitis capitata (Diptera: Tephritidae) that have received aromatherapy with ginger root oil. Florida Entomologist, 90: 175-179, 2007.

CÁCERES, C. Mass rearing of temperature sensitive genetic sexing strains in the Mediterranean fruit fly (Ceratitis capitata). Genetica, 116: 107–116, 2002.

CAYOL, J. P. Changes in sexual behavior and in some life history traits of tephritid species caused by mass-rearing processes. In: ALUJA, M.; NORRBOM, A. L. (Eds.). Fruit Flies (Diptera: Tephritidae): Phylogeny and Evolution of Behavior. Florida, USA: CRC Press, Boca Raton, 2000, cap. 31, p. 843-860.

CHAPMAN, T. et al. Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proceedings of the Royal Society of London, 265: 1879-1894, 1998.

CRUZ, C. D. Programa Genes: Diversidade Genética. 1. ed. Viçosa, MG: Editora da UFV, 2008. 278 p.

DHAKAL, P. et al. Isolating, amplifying and quantifying sperm DNA in Anastrepha suspensa (Diptera: Tephritidae). Florida Entomologist, 93: 63-72, 2010.

DE MEYER, M. Phylogeny of the genus Ceratitis (Dacinae: Ceratitidini). In: ALUJA, M.; NORRBOM, A. L. (Eds.). Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Florida, USA: CRC Press, Boca Raton, 2001, cap. 16, p. 409-428.

EBERHARD, W. G. Copulatory courtship and cryptic female choice in insects. Biological Reviews, 66: 1-31, 1991.

GASPARICH, G. E. et al. Analysis of mitochondrial DNA and development of PCR-based diagnostic molecular markers for Mediterranean fruit fly (Ceratitis capitata) populations. Insect Molecular Biology, 4: 61-67, 1995.

GILL, P.; JEFFREYS, A. J.; WERRET, D. J. Forensic application of DNA fingerprints. Nature, 318: 577-579, 1985.

HAJI, F. N. P. et al. Monitoramento de moscas-das-frutas no submédio do vale do São Francisco. In: MENEZES, A. M.; BARBOSA, F. R. (Eds.). Pragas da Mangueira: Monitoramento, Nível de Ação e Controle. Petrolina, PE: Embrapa Semi-Árido, 2005, cap. 4, p. 83-96.

HENDRICHS, J. et al. Medfly areawide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist, 85: 1-13, 2002.

IAEA - International Atomic Energy Agency. Genetic sexing of the Mediterranean fruit fly. STI/PUB/828. Panel Proceedings Series, IAEA. Vienna, Austria, 1990.

JANG, E. B. Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata. Journal of Insect Physiology, 41: 705-710, 1995.

JANG, E. B. et al. Mating induced changes in olfactory-mediated behavior of laboratory-reared normal, sterile, and wild female Mediterranean fruit flies (Diptera: Tephritidae) mated to conspecific males. Annals of the Entomological Society of America, 91: 139-144, 1998.

JANG, E. B. Physiology of mating behavior in Mediterranean fruit fly (Diptera: Tephritidae): chemoreception and male accessory gland fluids in female post-mating behavior. Florida Entomologist, 85: 89-93, 2002.

JUAN-BLASCO, M. et al. Molecular tools for sterile sperm detection to monitor Ceratitis capitata populations under SIT programmes. Pest Management Science, 69: 857-864, 2013a.

JUAN-BLASCO, M. et al. Improving the sterile sperm identification method for its implementation in the area-wide sterile insect technique program against Ceratitis capitata (Diptera: Tephritidae) in Spain. Journal of Economic Entomology, 106: 2541-2547, 2013b.

KLASSEN, W.; CURTIS, C. F. History of the sterile insect technique. In: DYCK, V. A.; HENDRICHS, J.; ROBINSON, A. S. (Eds.). Sterile Insect Technique: Principles and Practice in Area-wide Integrated Pest Management. Vienna, Austria: FAO/IAEA (Food and Agriculture Organization/International Atomic Energy Agency), 2005, cap. 1, p. 4-5.

KNIPLING, E.F. Sterile-male method of population control. Science, 130: 902-904, 1959.

KRAAIJEVELD, K.; CHAPMAN, T. Effects of male sterility on female remating in the Mediterranean fruit fly, Ceratitis capitata. Proceedings of the Royal Society of London B, 71: S209-S211, 2004.

LANCE, D. R. et al. Courtship among sterile and wild Ceratitis capitata (Diptera: Tephritidae) in field cages in Hawaii and Guatemala. Annalsof the Entomology Society of America, 93: 1179-1185, 2000.

LEE, S. G.; MCCOMBS, S. D.; SAUL, H. S. Sperm precedence of irradiated Mediterranean fruit fly males (Diptera: Tephritidae). Proceedings of the Hawaiian Entomological Society, 36: 47-59, 2003.

LIQUIDO, N. J.; MCQUATE, G.T.; SUITER, K. A. Medhost: An encyclopedic bibliography of the host plants of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), version 3.0. United States Department of Agriculture, Center for Plant Health Science and Technology, Raleigh, N.C., 2015. Disponível em: <https://medhost.cphst.org/>. Acesso em: 11 nov. 2022.

MORELLI, R. et al. Exposure of sterile Mediterranean fruit fly (Diptera: Tephritidae) males to ginger root oil reduces female remating. Journal of Applied Entomology, 137: 75-82, 2010.

MOSSINSON, S.; YUVAL, B. Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. Journal of Insect Physiology, 49: 561-567, 2003.

PAPADOPOULOS, N. T. et al. Effect of adult age, food, and time of day on sexual calling incidence of wild and mass-reared Ceratitis capitata males. Entomologia Experimentalis et Applicata, 89: 175-182, 1998.

PARANHOS, B. J. et al. Sterile medfly males of the tsl Vienna 8 genetic sexing strain improved mating performance with ginger root oil. In: 7TH INTERNATIONAL SYMPOSIUM ON FRUIT FLY OF ECONOMIC IMPORTANCE, 2006, Salvador, Proccedings… Salvador: SBPC, 2008, v. 1, p. 313-318.

PARANHOS, B. J. et al. Optimum dose of ginger root oil to treat sterile Mediterranean fruit fly males (Diptera: Tephritidae). Journal of Applied Entomology Hamburg, 137: 83-90, 2013.

PARKER, G. A. Sperm competition and its evolutionary consequences in the insects. Biological Reviews, 45: 525–567, 1970.

SAN ANDRÉS, V. et al. A novel molecular approach to assess mating success of sterile Medfly males in SIT programs. Journal of Economic Entomology, 100: 1444-1447, 2007.

SAUL, S. H.; MCCOMBS, S. D. Dynamics of sperm use in the Mediterranean fruit fly (Diptera: Tephritidae): reproductive fitness of multiple-mated females and sequentially mated males. Annals of the Entomological Society of America, 86: 198-202, 1993.

SHELLY, T. E. Mate choice by wild and mass-reared females of the Mediterranean fruit fly. Journal of Applied Entomology, 136: 238-240, 2011.

SILVA NETO, A. M. et al. Mass-rearing of Mediterranean fruit fly using low-cost yeast products produced in Brazil. Scientia Agricola, 69: 364-369, 2012.

SONG, S. D.; DREW, R. A. I.; HUGHES, J. M. Multiple paternity in a natural population of a wild tobacco fly, Bactrocera cacuminata (Diptera: Tephritidae), assessed by microsatellite DNA markers. Molecular Ecology, 16: 2353–2361, 2007.

SPANOS, L. et al. The mitochondrial genome of the Mediterranean fruit, Ceratitis capitata. Insect Molecular Biology, 9: 139-144, 2000.

TAYLOR, P. W. et al. Age-dependent insemination success of sterile Mediterranean fruit flies. Entomologia Experimentalis et Applicata, 98: 27-33, 2001.

TSUBAKI, Y. Mating systems of insects. In: HIGASHI, K.; UBUKATA, H.; TSUBAKI, Y. (Eds.). Dragonfly Mating Systems. Tokyo, JP: Tokai-Daigaku Shuppan-kai, 1988, v. 1, cap. 10, p. 246-285.

TSUBAKI, Y.; YAMAGISHI, M. “Longevity” of sperm within the female of the melon fly, Dacus cucurbitae (Diptera: Tephritidae), and its relevance to sperm competition. Journal of Insect Behavior, 4: 243-250, 1991.

VERA, M. T. et al. Potential geographical distribution of the Mediterranean fruit fly, Ceratitis capitata (Diptera: Tephritidae), with emphasis on Argentina and Australia. Environmental Entomology, 31: 1009-1022, 2002.

YUVAL, B. et al. Nutritional reserves regulate male participation in Mediterranean fruit fly leks. Ecological Entomology, 23: 211-215, 1998.

YUVAL, B. et al. Effects of post-teneral nutrition on reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Florida Entomologist, 85: 165-170, 2002.

YUVAL, B. et al. Breakfast of champions or kiss of death? Survival and sexual performance of protein-fed, sterile Mediterranean fruit flies (Diptera: Tephritidae). Florida Entomologist, 90: 115-122, 2007.

WALDER, J. M. M. Técnica do inseto estéril – controle genético. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância Econômica no Brasil: Conhecimento Básico e Aplicado. Ribeirão Preto, SP: Holos Editora, 2000, cap. 19, p. 151-158.

ZHOU, Q.; UNTALAN, P. M.; HAYMER, D. S. Repetitive A-T rich DNA sequences from the Y chromosome of the Mediterranean fruit fly, Ceratitis capitata. Genome, 43: 434-438, 2000.

ZUCCHI, R. A.; MORAES, R. C. B. Fruit flies in Brazil - Hosts and parasitoids of the Mediterranean fruit fly. ESALQ/USP, 2021. Disponível em: <http://www.lea.esalq.usp.br/ceratitis>. Acesso em: 11 nov. 2022.

Downloads

Published

18-07-2023

Issue

Section

Agronomy