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Remating behavior in Anastrepha fraterculus (Diptera: Tephritidae) females is affected by male juvenile hormone analog treatment but not by male sterilization

Published online by Cambridge University Press:  23 January 2013

S. Abraham ,
M.C. Liendo ,
F. Devescovi ,
P.A. Peralta ,
V. Yusef ,
J. Ruiz ,
J.L. Cladera ,
M.T. Vera  and
D.F. Segura
S. Abraham*
Affiliation:
Cátedra de Terapéutica Vegetal, Departamento de Sanidad Vegetal de la Facultad de Agronomía y Zootecnia de la UNT, Tucumán, Argentina CONICET, Buenos Aires, Argentina
M.C. Liendo
Affiliation:
CONICET, Buenos Aires, Argentina Instituto de Genética ‘E.A. Favret’, INTA Castelar, Buenos Aires, Argentina
F. Devescovi
Affiliation:
CONICET, Buenos Aires, Argentina Instituto de Genética ‘E.A. Favret’, INTA Castelar, Buenos Aires, Argentina
P.A. Peralta
Affiliation:
Instituto de Genética ‘E.A. Favret’, INTA Castelar, Buenos Aires, Argentina
V. Yusef
Affiliation:
Centro Atómico Ezeiza, Comisión Nacional de Energía Atómica (CAE, CNEA), Buenos Aires, Argentina
J. Ruiz
Affiliation:
CONICET, Buenos Aires, Argentina Estacion Experimental Agroindustrial Obispo Colombres, Tucumán, Argentina
J.L. Cladera
Affiliation:
Instituto de Genética ‘E.A. Favret’, INTA Castelar, Buenos Aires, Argentina
M.T. Vera
Affiliation:
Cátedra de Terapéutica Vegetal, Departamento de Sanidad Vegetal de la Facultad de Agronomía y Zootecnia de la UNT, Tucumán, Argentina CONICET, Buenos Aires, Argentina
D.F. Segura
Affiliation:
CONICET, Buenos Aires, Argentina Instituto de Genética ‘E.A. Favret’, INTA Castelar, Buenos Aires, Argentina
*
* Author for correspondence Phone: +54 0381 4390040 E-mail: solanaabraham@yahoo.com.ar
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Abstract

The sterile insect technique (SIT) has been proposed as an area-wide method to control the South American fruit fly, Anastrepha fraterculus (Wiedemann). This technique requires sterilization, a procedure that affects, along with other factors, the ability of males to modulate female sexual receptivity after copulation. Numerous pre-release treatments have been proposed to counteract the detrimental effects of irradiation, rearing and handling and increase SIT effectiveness. These include treating newly emerged males with a juvenile hormone mimic (methoprene) or supplying protein to the male's diet to accelerate sexual maturation prior to release. Here, we examine how male irradiation, methoprene treatment and protein intake affect remating behavior and the amount of sperm stored in inseminated females. In field cage experiments, we found that irradiated laboratory males were equally able to modulate female remating behavior as fertile wild males. However, females mated with 6-day-old, methoprene-treated males remated more and sooner than females mated with naturally matured males, either sterile or wild. Protein intake by males was not sufficient to overcome reduced ability of methoprene-treated males to induce refractory periods in females as lengthy as those induced by wild and naturally matured males. The amount of sperm stored by females was not affected by male irradiation, methoprene treatment or protein intake. This finding revealed that factors in addition to sperm volume intervene in regulating female receptivity after copulation. Implications for SIT are discussed.

Keywords

South American fruit flySITmethoprenesperm storage
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 3 , June 2013 , pp. 310 - 317
Copyright
Copyright © Cambridge University Press 2013

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References

Abraham, S., Goane, L., Rull, J., Cladera, J., Willink, E. & Vera, M.T. (2011a) Multiple mating in Anastrepha fraterculus females and its relationship with fecundity and fertility. Entomologia Experimentalis et Applicata 141, 15–24.CrossRefGoogle Scholar
Abraham, S., Goane, L., Cladera, J. & Vera, M.T. (2011b) Effects of male nutrition on sperm storage and remating behavior in wild and laboratory Anastrepha fraterculus (Diptera: Tephritidae) females. Journal of Insect Physiology 57, 1501–1509.Google Scholar
Abraham, S., Cladera, J., Goane, L. & Vera, M.T. (2012) Factors affecting Anastrepha fraterculus female receptivity modulation by accessory gland products. Journal of Insect Physiology 58, 1–6.CrossRefGoogle ScholarPubMed
Allinghi, A., Gramajo, C., Willink, E. & Vilardi, J.C. (2007) Induction of sterility in Anastrepha fraterculus (Diptera: Tephritidae) by gamma radiation. Florida Entomologist 90, 96–102.Google Scholar
Aluja, M., Jácome, I. & Macías-Ordóñez, R. (2001) Effects of adult nutrition on male sexual performance in four neotropical fruit fly species of the genus Anastrepha (Diptera: Tephritidae). Journal of Insect Behavior 14, 759–775.Google Scholar
Aluja, M., Pérez-Staples, D., Sivinski, J., Sánchez, A. & Piñero, J. (2008) Effects of male condition on fitness in two tropical tephritid flies with contrasting life histories. Animal Behaviour 76, 1997–2009.CrossRefGoogle Scholar
Aluja, M., Rull, J., Sivinski, J., Trujillo, G. & Pérez-Staples, D. (2009) Male and female condition influence mating performance and sexual receptivity in two tropical fruit flies (Diptera: Tephritidae) with contrasting life histories. Journal of Insect Physiology 55, 1091–1098.Google Scholar
Baker, R.H., Denniff, M., Futerman, P., Fowler, K., Pomiankowski, A. & Chapman, T. (2003) Accessory gland size influences time to sexual maturity and mating frequency in the stalk-eyed fly, Cyrtodiopsis dalmanni . Behavioral Ecology 14, 607–611.CrossRefGoogle Scholar
Bloem, K., Bloem, S., Rizzo, N. & Chambers, D. (1993) Female medfly refractory period: effect of male reproductive status. pp. 189–190 in Aluja, M. & Liedo, P. (Eds) Fruit Flies: Biology and Management. New York, Springer-Verlag.CrossRefGoogle Scholar
Briceño, R.D. & Eberhard, W.G. (2002) Decisions during courtship by male and female medflies (Diptera, Tephritidae): correlated changes in male behaviour and female acceptance criteria in mass-reared flies. Florida Entomologist 85, 14–31.Google Scholar
del Barco-Trillo, J. (2011) Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. Journal of Evolutionary Biology 24, 1706–1714.Google Scholar
Gage, A.R. & Barnard, C.J. (1996) Male cricket increase sperm number in relation to competition and female size. Behavioral Ecology and Sociobiology 38, 349–353.CrossRefGoogle Scholar
Gage, M.J.G. (1991) Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit fly. Animal Behaviour 42, 1036–1037.Google Scholar
Gage, M.J.G. & Baker, R.R. (1991) Ejaculate size varies with socio-sexual situation in an insect. Ecological Entomology 16, 331–337.CrossRefGoogle Scholar
Gavriel, S., Gazit, Y. & Yuval, B. (2009) Remating by female Mediterranean fruit flies (Ceratitis capitata, Diptera: Tephritidae): temporal patterns and modulation by male condition. Journal of Insect Physiology 55, 637–642.Google Scholar
Haq, I., Cáceres, C., Hendrichs, J., Teal, P., Wornoayporn, V., Stauffer, C. & Robinson, A.S. (2010) Effects of the juvenile hormone analogue methoprene and dietary protein on male melon fly Bactrocera cucurbitae (Diptera: Tephritidae) mating success. Journal of Insect Physiology 56, 1503–1509.CrossRefGoogle Scholar
Harmer, A.M.T., Radhakrishnan, P. & Taylor, P.W. (2006) Remating inhibition in female Queensland fruit flies: effects and correlates of sperm storage. Journal of Insect Physiology 52, 179–186.Google Scholar
Hendrichs, J., Robinson, A.S., Cayol, J.P. & Enkerlin, W. (2002) Medfly areawide sterile insect technique programs for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist 85, 1–13.Google Scholar
Hendrichs, M.A., Wornoayporn, V., Katsoyannos, B. & Hendrichs, J. (2007) Quality control method to measure predator evasion in wild and mass-reared Mediterranean fruit flies (Diptera: Tephritidae). Florida Entomologist 90, 64–70.Google Scholar
InfoStat (2009) Manual del Usuario, 1st edition. Grupo InfoStat, FCA, Universidad Nacional de Córdoba. Argentina, Editorial Brujas.Google Scholar
Jaldo, H.E. (2001) Estudios biológicos y poblacionales de Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae). PhD Thesis, Universidad Nacional de Tucumán, Argentina.Google Scholar
Jaldo, H.E., Gramajo, M.C. & Willink, E. (2001) Mass rearing of Anastrepha fraterculus (Diptera: Tephritidae): a preliminary strategy. Florida Entomologist 84, 716–718.Google Scholar
Kelly, C.D. & Jennions, M.D. (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biological Review of the Cambridge Philosophical Society 86, 863–884.Google Scholar
Liendo, M.C., Devescovi, F., Bachmann, G.E., Utgés, M.E., Abraham, S., Vera, M.T., Lanzavecchia, S.B., Bouvet, J.P., Gómez-Cendra, P.V., Hendrichs, J., Teal, P.E.A., Cladera, J.L. & Segura, D.F. (2012) Precocious sexual signaling and mating in Anastrepha fraterculus (Diptera: Tephritidae) sterile males achieved through juvenile hormone treatment and protein supplements. Bulletin of Entomological Research, in press (doi: 10.1017/S0007485312000442).Google ScholarPubMed
Liimatainen, J., Hoikkala, A. & Shelly, T. (1997) Courtship behavior in Ceratitis capitata (Diptera: Tephritidae) comparison of wild and mass-reared males. Annals of the Entomological Society of America 90, 836–843.Google Scholar
Lima, I.S.D., Howse, P.E. & Salles, L.A.B. (1994) Reproductive behaviour of the South American fruit fly Anastrepha fraterculus (Diptera: Tephritidae): laboratory and field studies. Physiological Entomology 19, 271–277.CrossRefGoogle Scholar
Lux, S.A., Vilardi, J.C., Liedo, P., Gaggl, K., Calcagno, G.E., Munyiri, F.N., Vera, M.T. & Manso, F. (2002) Effects of irradiation on the courtship behavior of medfly (Diptera, Tephritidae) mass reared for the sterile insect technique. Florida Entomologist 85, 102–112.CrossRefGoogle Scholar
Malavasi, A., Morgante, J.S. & Prokopy, R.J. (1983) Distribution and activities of Anastrepha fraterculus (Diptera: Tephritidae) flies on host and non host trees. Annals of the Entomological Society of America 76, 286–292.Google Scholar
Mossinson, S. & Yuval, B. (2003) Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and new synthesis proposed. Journal of Insect Physiology 49, 561–567.Google Scholar
Norrbom, A.L. (2004) Host plant database for Anastrepha and Toxotripana (Diptera: Tephritidae: Toxotripanini). Available at: http://www.sel.barc.usda.gov/diptera/tephriti/tephriti.htm (accessed 3 December 2012).Google Scholar
Ortíz, G. (1999) Potential use of the sterile insect technique against the South American fruit fly. pp. 121–130 in IAEA (Ed.) The South American Fruit Fly, Anastrepha fraterculus (Wied.): Advances in Artificial Rearing, Taxonomic Status and Biological Studies: Proceedings of a workshop organized by the Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture and held in Viña del Mar, Chile, 1–2 November 1996. Vienna, International Atomic Energy Agency.Google Scholar
Pereira, R., Sivinski, J. & Teal, P.E.A. (2009) Influence of methoprene and dietary protein on male Anastrepha suspensa (Diptera: Tephritidae) mating aggregations. Journal of Insect Physiology 55, 328–335.Google Scholar
Pereira, R., Yuval, B., Liedo, P., Teal, P.E.A., Shelly, T.E., McInnis, D.O. & Hendrichs, J. (2011) Improving sterile male performance in support of programmes integrating the sterile insect technique against fruit flies. Journal of Applied Entomology doi: 10.1111/j.1439-0418.2011.01664.x.Google Scholar
Pérez-Staples, D., Aluja, M., Macías-Ordóñez, R. & Sivinski, J. (2008a) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua . Behavioral Ecology and Sociobiology 62, 1333–1340.Google Scholar
Pérez-Staples, D., Harmer, A.M.T., Collins, S.R. & Taylor, P.W. (2008b) Potential for pre-release diet supplements to increase the sexual performance and longevity of male Queensland fruit flies. Agricultural and Forest Entomology 10, 255–262.CrossRefGoogle Scholar
Pérez-Staples, D., Weldon, C.W., Smallridge, C. & Taylor, P.W. (2009) Pre-release feeding on yeast hydrolysate enhances sexual competitiveness of sterile male Queensland fruit flies in field cages. Entomologia Experimentalis et Applicata 131, 159–166.Google Scholar
Petit-Marty, N., Vera, M.T., Calcagno, G., Cladera, J.L., Segura, D.F., Allinghi, A., Rodriguero, M., Gómez Cendra, P., Viscarret, M.M. & Vilardi, J.C. (2004) Sexual behavior and mating compatibility among four populations of Anastrepha fraterculus (Diptera: Tephritidae) from Argentina. Annals of the Entomological Society of America 97, 1320–1327.Google Scholar
Prabhu, V., Pérez-Staples, D. & Taylor, P.W. (2008) Protein: carbohydrate ratios promoting sexual activity and longevity of male Queensland fruit flies. Journal of Applied Entomology doi: 10.1111/j.1439-0418.2007.01265.x.Google Scholar
Rull, J., Brunel, O. & Mendez, M.E. (2005) Mass rearing history negatively affects mating success of male Anastrepha ludens (Diptera: Tephritidae) reared for the sterile insect technique. Journal of Economical Entomology 98, 1510–1516.Google Scholar
Segura, D.F., Cáceres, C., Vera, M.T., Wornoayporn, V., Islam, A., Teal, P.E.A., Cladera, J.L., Hendrichs, J. & Robinson, A.S. (2009) Enhancing mating performance after juvenile hormone treatment in Anastrepha fraterculus: a differential response in males and females acts as a physiological sexing system. Entomologia Experimentalis et Applicata 131, 75–84.Google Scholar
Segura, D.F., Utges, M.E., Liendo, M.C., Rodríguez, M.F., Devescovi, F., Vera, M.T., Teal, P.E.A. & Cladera, J.L. (2010) Methoprene treatment reduces the pre-copulatory period in Anastrepha fraterculus (Diptera: Tephritidae) sterile males. Journal of Applied Entomology doi: 10.1111/j.1439-0418.2010.01534.x.Google Scholar
Seo, S.T., Vargas, R.I., Gilmore, J.E., Kurashima, R.S. & Fujimoto, M.S. (1990) Sperm transfer in normal and gamma-irradiated, laboratory-reared Mediterranean fruit flies (Diptera: Tephritidae). Journal of Economical Entomology 83, 1949–1953.Google Scholar
Shelly, T.E. & Kennelly, S. (2002) Influence of male diet on male mating success and longevity and female remating in the Mediterranean fruit fly (Diptera: Tephritidae) under laboratory condition. Florida Entomologist 85, 572–578.Google Scholar
Taylor, P.W. & Yuval, B. (1999) Postcopulatory sexual selection in Mediterranean fruit flies, Ceratitis capitata: advantages for large and protein-fed males. Animal Behaviour 58, 247–254.Google Scholar
Taylor, P.W., Kaspi, R., Mossinson, S. & Yuval, B. (2001) Age-dependent insemination success of sterile Mediterranean fruit flies. Entomologia Experimentalis et Applicata 98, 27–33.CrossRefGoogle Scholar
Teal, P.E.A., Gómez-Simuta, Y. & Proveaux, A.T. (2000) Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. Proceedings of the National Academy of Sciences USA 97, 3708–3712.Google Scholar
Teal, P.E.A., Gómez-Simuta, Y., Dueben, B.D., Holler, T.C. & Olson, S.R. (2007) Improving the efficacy of the sterile insect technique for fruit flies by incorporation of hormone and dietary supplements into adult holding protocols. pp. 163–173 in Vreysen, M.J.B., Robinson, A.S., Hendrichs, J. (Eds) Area-wide Control of Insect Pests: from Research to Field Implementation. Dordrecht, The Netherlands, Springer.Google Scholar
Teal, P.E.A., Pereira, R., Segura, D.F., Haq, I., Gómez-Simuta, Y., Robinson, A.S. & Hendrichs, J. (2011) Methoprene and protein supplements accelerate reproductive development and improve mating success of male tephritid flies. Journal of Applied Entomology doi: 10.1111/j.1439-0418.2010.01606.x.Google Scholar
Vera, M.T., Cladera, J.L., Calcagno, G., Vilardi, J.C., McInnis, D.O., Stolar, E., Segura, D.F., Petit-Marty, N., Krsticevic, F., Gómez Cendra, P., Rodriguero, M., Barborini, K., Heer, T., Allinghi, A., Bonpland, G., Hansen, L. & Segade, G. (2003) Remating of wild Ceratitis capitata (Diptera: Tephritidae) females in field cages. Annals of the Entomological Society of America 96, 563–570.Google Scholar
Yuval, B., Kaspi, R., Field, S.A., Blay, S. & Taylor, P. (2002) Effects of post-teneral nutrition on reproductive success of male Mediterranean fruit flies (Diptera: Tephritidae). Florida Entomologist 85, 165–170.CrossRefGoogle Scholar
Yuval, B., Maor, M., Levy, K., Kaspi, R., Taylor, P.T. & Shelly, T. (2007) Breakfast of champions or kiss or death? Survival and sexual performance of protein-fed, sterile Mediterranean fruit flies (Diptera: Tephritidae). Florida Entomologist 90, 115–122.Google Scholar