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Oviposition after sex: mated Anastrepha ludens (Diptera: Tephritidae) females increase oviposition without receiving an ejaculate

Published online by Cambridge University Press:  22 April 2021

M. Reyes-Hernández
Affiliation:
Universidad Autónoma de Guadalajara, Av. Patria 1201, Col. Lomas del Valle, C.P. 45129, Zapopan, Jalisco, México INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
G. Córdova-García
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
F. Díaz-Fleischer
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
N. Flores-Estévez
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
D. Pérez-Staples*
Affiliation:
INBIOTECA, Universidad Veracruzana, Av. de las Culturas Veracruzanas No.101, Col. E. Zapata, C.P. 91090, Xalapa, Veracruz, México
*
*Corresponding author. Email: [email protected]

Abstract

Mating and receiving ejaculate can alter female insect physiology and postcopulatory behaviour. During mating, females receive both internal and external stimuli and different components in the ejaculate. In insects, these components consist mostly of sperm and male accessory gland secretions. Some of the most important changes associated with receiving male accessory gland secretions are a reduction in female sexual receptivity and an increase in oviposition. However, a clear function for these molecules has not been found in the Mexican fruit fly Anastrepha ludens (Loew) (Diptera: Tephritidae). Here, we tested how the stimulus of mating, receiving a full ejaculate, or only receiving accessory gland secretions can influence ovarian development and oviposition. Our results indicate that the stimulus of mating per se is enough to induce oviposition and increase egg laying in females even if ejaculate is not received, whereas receiving only accessory gland secretions does not increase ovarian development and is not enough to induce oviposition or increase egg production. Further research on the internal and external copulatory courtship of A. ludens will increase our understanding of the role of these secretions in stimulating oviposition independent of ejaculate effects. A biological function for male accessory gland secretions on female behaviour for A. ludens still needs to be found.

Type
Research Papers
Copyright
© The Author(s), 2021. Published by Cambridge University Press on behalf of the Entomological Society of Canada

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Footnotes

Subject editor: Maya Evenden

References

Abraham, S., Caldera, J., Goane, L., and Vera, M.T. 2012. Factors affecting Anastrepha fraterculus female receptivity modulation by accessory gland products. Journal of Insect Physiology, 58: 16.CrossRefGoogle ScholarPubMed
Abraham, S., Lara-Pérez, L.A., Rodríguez, C., Contreras-Navarro, Y., Núñez-Beverido, N., Ovruski, S., and Pérez-Staples, D. 2016. The male ejaculate as inhibitor of female remating in two tephritid flies. Journal of Insect Physiology, 88: 4047.CrossRefGoogle ScholarPubMed
Abraham, S., Núñez-Beverido, N., Contreras-Navarro, Y., and Pérez-Staples, D. 2014. Female receptivity in Anastrepha ludens (Diptera: Tephritidae) is not modulated by male accessory gland products. Journal of Insect Physiology, 70: 4148.CrossRefGoogle Scholar
Aisenberg, A. and Costa, F.G. 2005. Females mated without sperm transfer maintain high sexual receptivity in the wolf spider Scizocosa malitiosa. Ethology, 111: 545558.CrossRefGoogle Scholar
Aluja, M., Dıaz-Fleischer, F., Papaj, D.R., Lagunes, G., and Sivinski, J. 2001. Effects of age, diet, female density, and the host resource on egg load in Anastrepha ludens and Anastrepha obliqua (Diptera: Tephritidae). Journal of Insect Physiology, 47: 975988.CrossRefGoogle Scholar
Aluja, M., Pinero, J., Jacome, I., Diaz-Fleischer, F., and Sivinski, J. 2000. Behavior of flies of the genus Anastrepha . In Fruit Flies (Tephritidae): phylogeny and evolution of behavior. Edited by M. Aluja and A.L. Norrbom. CRC Press, DelRay Beach, Florida, United States of America. Pp. 375408.Google Scholar
Aluja, M., Rull, J., Sivinski, J., Trujillo, G., and 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: 10911098.CrossRefGoogle ScholarPubMed
Avila, F.W., Sirot, L.K., LaFlame, A., Rubistein, C.D., and Wolfer, M.F. 2011. Insect seminal fluid proteins: identification and function. Annual Review of Entomology, 56: 2140.CrossRefGoogle ScholarPubMed
Baena Hurtado, M.L. 2009. Efectos de la cópula y el tamaño del macho sobre el comportamiento de ovipostura en la mosca estercolera Archisepsis diversiformis (Diptera: Sepsidae). Revista de Biología Tropical, 57: 239250.Google Scholar
Ben-Yosef, M., Jurkevitch, E., and Yuval, B. 2008. Effect of bacteria on nutritional status and reproductive success of the Mediterranean fruit fly Ceratitis capitata . Physiological Entomology, 33: 145154.CrossRefGoogle Scholar
Brent, C.S. and Hull, J.J. 2014. Characterization of male-derived factors inhibiting female sexual receptivity in Lygus hesperus . Journal of Insect Physiology, 60: 104110.CrossRefGoogle ScholarPubMed
Briceño, R.D., Orozco, D., Luis, Q.J., Hanson, P., and Hernández, M. 2011. Copulatory behaviour and the process of intromission in Anastrepha ludens (Diptera: Tephritidae). Revista de Biología Tropical, 59: 291297.Google Scholar
Carey, J.R., Liedo, P., Müller, H.G., Wang, J.L., Senturk, D., and Harshman, L. 2005. Biodemography of a long-lived tephritid: reproduction and longevity in a large cohort of female Mexican fruit flies, Anastrepha ludens . Experimental Gerontology, 40: 79800.CrossRefGoogle Scholar
Craig, G.B. 1967. Mosquitoes: female monogamy induced by male accessory gland substance. Science, 156: 14991501.CrossRefGoogle ScholarPubMed
Cury, K.M., Prud’homme, B., and Gompel, N. 2019. A short guide to insect oviposition: when, where and how to lay an egg. Journal of Neurogenetics, 33: 7589. https://doi.org/10.1080/01677063.2019.1586898.CrossRefGoogle Scholar
Díaz-Fleischer, F. and Aluja, M. 2003. Behavioural plasticity in relation to egg and time limitation: the case of two fly species in the genus Anastrepha (Diptera: Tephritidae). Oikos, 100: 125133.CrossRefGoogle Scholar
Eberhard, W.G. 2005. Threading a needle with reinforced thread: intromission in Ceratitis capitata (Diptera, Tephritidae). The Canadian Entomologist, 137: 174181.CrossRefGoogle Scholar
Fernández, N.M. and Klowden, M.J. 1995. Male accessory gland substances modify the host-seeking behavior of gravid Aedes aegypti mosquitoes. Journal of Insect Physiology, 4: 1965–970.Google Scholar
Fricke, C., Wigby, S., Hobbs, R., and Chapman, T. 2009. The benefits of male ejaculate sex peptide transfer in Drosophila melanogaster . Journal of Evolutionary Biology, 22: 275286.CrossRefGoogle ScholarPubMed
Fritz, A.H. and Turner, F.R. 2002. A light and electron microscopical study of the spermathecae and ventral receptacle of Anastrepha suspensa (Diptera: Tephritidae) and implications in female influence of sperm storage. Arthropod Structure & Development, 30: 293313.CrossRefGoogle ScholarPubMed
Gillott, C. 2003. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology, 48: 163184.CrossRefGoogle ScholarPubMed
Gou, B., Liu, Y., Guntur, A.R., Stern, U., and Yang, C.H. 2014. Mechanosensitive neurons on the internal reproductive tract contribute to egg-laying-induced acetic acid attraction in Drosophila . Cell Reports, 9: 522530. https://doi.org/10.1016/j.celrep.2014.09.033.CrossRefGoogle ScholarPubMed
Helinski, M.E., Deewatthanawong, P., Sirot, L.K., Wolfner, M.F., and Harrington, L.C. 2012. Duration and dose-dependency of female sexual receptivity responses to seminal fluid proteins in Aedes albopictus and Ae. aegypti mosquitoes. Journal of Insect Physiology, 58: 13071313.CrossRefGoogle ScholarPubMed
Hendrichs, J., Franz, G., and Rendon, P. 1995. Increased effectiveness and applicability of the sterile insect technique through male-only releases for control of Mediterranean fruit flies during fruiting seasons. Journal of Applied Entomology, 119: 371377. https://doi.org/10.1111/j.1439-0418.1995.tb01303.x.CrossRefGoogle Scholar
Hendrichs, J., Robinson, A.S., Cayol, J.P., and Enkerlin, W. 2002. Medfly area-wide sterile insect technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist, 85: 113.CrossRefGoogle Scholar
Imamura, M., Haino-Fukushima, K., Aigaki, T., and Fuyama, Y. 1998. Ovulation stimulating substances in Drosophila biarmipes males: their origin, genetic variation in the response of females, and molecular characterization. Insect Biochemistry and Molecular Biology, 28: 365372.CrossRefGoogle ScholarPubMed
Jang, E. 1995. Effects of mating and accessory gland injections on olfactory-mediated behavior in the female Mediterranean fruit fly, Ceratitis capitata . Journal of Insect Physiology, 41: 705710.CrossRefGoogle Scholar
Jang, E.B., McInnis, D.O., Kurashima, R., and Carvalho, L.A. 1999. Behavioural switch of female Mediterranean fruit fly, Ceratitis capitata: mating and oviposition activity in outdoor field cages in Hawaii. Agricultural and Forest Entomology, 1: 179184.CrossRefGoogle Scholar
Judson, C.L. 1967. Feeding and oviposition behavior in the mosquito Aedes aegypti (L.). I. Preliminary studies of physiological control mechanisms. The Biological Bulletin, 133: 369377.CrossRefGoogle ScholarPubMed
Knipling, E.F. 1955. Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology, 48: 459462.CrossRefGoogle Scholar
Kuba, H. and Ito, Y. 1993. Remating inhibition in the melon fly, Bactrocera (= Dacus) cucurbitae (Diptera: Tephritidae): copulation with spermless males inhibits female remating. Journal of Ethology, 11: 2328.CrossRefGoogle Scholar
Lance, D.R. and McInnis, D.O. 2005. Biological basis of the sterile insect technique. In Sterile insect technique: principles and practice in area-wide integrated pest management. Edited by V.A. Dyck, J. Hendricks, and A.S. Robinson. Springer, Dordrecht, The Netherlands. Pp: 6594.Google Scholar
Lee, J.J. and Klowden, M.J. 1999. A male accessory gland protein that modulates female mosquito (Diptera: Culicidae) host-seeking behavior. Journal of the American Mosquito Control Association, 15: 47.Google ScholarPubMed
Lentz, A.J., Miller, J.R., Spencer, J.L., and Keller, J.E. 2009. Effect of male accessory gland extracts on female oviposition and sexual receptivity of the Caribbean fruit fly (Diptera: Tephritidae). Florida Entomologist, 92: 415420.Google Scholar
Liu, H. and Kubli, E. 2003. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster . Proceedings of the National Academy of Sciences, 100: 99299933.CrossRefGoogle ScholarPubMed
Loher, W. 1979. The influence of prostaglandin E2 on oviposition in Teleogryllus commodus . Entomologia Experimentalis et Applicata, 25: 107109. https://doi.org/10.1111/j.1570-7458.1979.tb02853.x.CrossRefGoogle Scholar
Lung, O., Kuo, L., and Wolfner, M.F. 2001. Drosophila males transfer antibacterial proteins from their accessory gland and ejaculatory duct to their mates. Journal of Insect Physiology, 47: 617622.CrossRefGoogle ScholarPubMed
Markow, T.A. 2015. Drosophila reproduction: molecules meet morphology. Proceedings of the National Academy of Sciences, 112: 81688169.CrossRefGoogle ScholarPubMed
Meza, J.S., Arredondo, J., Orozco, D., and Pérez-Staples, D. 2014. Disparity in sexual behaviour between wild and mass-reared Mexican fruit flies. Physiological Entomology, 39: 263270.CrossRefGoogle Scholar
Miyatake, T., Chapman, T., and Partridge, L. 1999. Mating-induced inhibition of remating in female Mediterranean fruit flies, Ceratitis capitata . Journal of Insect Physiology, 45: 10211028.CrossRefGoogle ScholarPubMed
Mossinson, S. and Yuval, B. 2003. Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. Journal of Insect Physiology, 49: 561567.CrossRefGoogle Scholar
Orozco, D., Hernández, M.R., Meza, J.S., and Quintero, J.L. 2013. Do sterile females affect the sexual performance of sterile males of Anastrepha ludens (Diptera: Tephritidae)? Journal of Applied Entomology, 137: 321326. https://doi.org/10.1111/j.1439-0418.2012.01748.x.CrossRefGoogle Scholar
Orozco-Dávila, D., Adriano-Anaya, M.d.L., Quintero-Fong, L., and Salvador-Figueroa, M. 2015. Sterility and sexual competitiveness of Tapachula-7 Anastrepha ludens males irradiated at different doses. PLOS One, 10: e0135759.CrossRefGoogle ScholarPubMed
Orozco-Dávila, D., Quintero, L., Hernández, E., Solis, E., Artiaga, T., Hernández, R., et al. 2017. Mass rearing and sterile insect releases for the control of Anastrepha spp. pests in Mexico: a review. Entomologia Experimental et Applicata, 164: 176187. https://doi.org/10.1111/eea.12581.CrossRefGoogle Scholar
Peretti, A.V. and Aisenberg, A. (editors). 2015. Cryptic female choice in arthropods: patterns, mechanisms and perspectives. Springer International Publishing, Cham, Switzerland.Google Scholar
Pérez-Staples, D., Córdova-García, G., and Aluja, M. 2014. Sperm dynamics and cryptic male choice in tephritid flies. Animal Behaviour, 89: 131139. https://doi.org/10.1016/j.anbehav.2013.12.016.CrossRefGoogle Scholar
Perry, J.C., Sirot, L., and Wigby, S. 2013. The seminal symphony: how to compose an ejaculate. Trends in Ecology & Evolution, 28: 414422.CrossRefGoogle ScholarPubMed
R Core Team. 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.R-project.org/ Google Scholar
Radhakrishnan, P., Nair, S., Raftos, D., and Taylor, P.W. 2008. Transfer and fate of male ejaculate in female Queensland fruit flies. Physiological Entomology, 33: 302309. https://doi.org/10.1111/j.1365-3032.2008.00631.x.CrossRefGoogle Scholar
Radhakrishnan, P., Pérez-Staples, D., Weldon, C.W., and Taylor, P.W. 2009. Multiple mating and sperm depletion in male Queensland fruit flies: effects on female remating behaviour. Animal Behaviour, 78: 839846.CrossRefGoogle Scholar
Radhakrishnan, P. and Taylor, P.W. 2007. Seminal fluids mediate sexual inhibition and short copula duration in mated female Queensland fruit flies. Journal of Insect Physiology, 53: 74145.CrossRefGoogle ScholarPubMed
Reyes-Hernández, M. and Pérez-Staples, D. 2017. Mating senescence and male reproductive organ size in the Mexican fruit fly. Physiological Entomology, 42: 2635. https://doi.org/10.1111/phen.12160.CrossRefGoogle Scholar
Robacker, D.C., Ingle, S.J., and Hart, W.G. 1985. Mating frequency and response to male produced pheromone by virgin and mated females of the Mexican fruit fly. Southwestern Entomologist, 10: 215221.Google Scholar
Robinson, A.S., Cayol, J.P., and Hendrichs, J. 2002. Recent findings on medfly sexual behavior: implications for SIT. Florida Entomologist, 85: 171181.CrossRefGoogle Scholar
Rodríguez, R. 2015. Mating is a give-and-take of influence and communication between the sexes. In Cryptic female choice in arthropods: patterns, mechanisms and perspectives. Edited by A.V. Peretti and A. Aisenberg. Springer International Publishing, Cham, Switzerland. Pp. 479496.CrossRefGoogle Scholar
Shutt, B., Stables, L., Aboagye, A.F., Moran, J., and Tripet, F. 2010. Male accessory gland proteins induce female monogamy in anopheline mosquitoes. Medical and Veterinary Entomology, 24: 9194.CrossRefGoogle ScholarPubMed
Sirot, L.K., LaFlamme, B.A., Sitnik, J.L., Rubinstein, D., Avila, F.W., Chow, C.Y., and Wolfner, M.F. 2009. Molecular social interactions: Drosophila melanogaster seminal fluid protein as a case study. Advances in Genetics, 68: 2356.CrossRefGoogle ScholarPubMed
Sirot, L.K., Poulson, R.L., McKenna, M.C., Girnary, H., Woflner, M.F., and Harrington, L.C. 2008. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochemistry and Molecular Biology, 38: 176189.CrossRefGoogle ScholarPubMed
Stanley-Samuelson, D.W. 1994. Prostaglandins and related eicosanoids in insects. Advances in Insect Physiology, 24: 115212. https://doi.org/10.1016/S0065-2806(08)60083-1.CrossRefGoogle Scholar
Thomas, D.B., Leal, S.N., and Conwat, H.E. 2014. Copula duration, insemination, and sperm allocation in Anastrepha ludens (Diptera: Tephritidae). Annals of the Entomological Society of America, 107: 858865.CrossRefGoogle Scholar
Villarreal, S.M., Pitcher, S., Helinski, M.E., Johnson, L., Wolfner, M.F., and Harrington, L.C. 2018. Male contributions during mating increase female survival in the disease vector mosquito Aedes aegypti . Journal of Insect Physiology, 108: 19.CrossRefGoogle ScholarPubMed
Wolfner, M.F. 2002. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila . Heredity, 88: 8593.CrossRefGoogle ScholarPubMed
Worthington, A.M., Jurenka, R.A., and Kelly, C.D. 2015. Mating for male-derived prostaglandin: a functional explanation for the increased fecundity of mated female crickets? Journal of Experimental Biology, 218: 27202727. https://doi.org/10.1242/jeb.121327.Google ScholarPubMed
Xu, J. and Wang, Q. 2011. Seminal fluid reduces female longevity and stimulates egg production and sperm trigger oviposition in a moth. Journal of Insect Physiology, 57: 385390.CrossRefGoogle Scholar
Yamane, T. and Miyatake, T. 2010. Induction of oviposition by injection of male-derived extracts in two Callosobruchus species. Journal of Insect Physiology, 56: 17831788.CrossRefGoogle ScholarPubMed
Yu, J.F., Li, C., Xu, J., Liu, J.H., and Ye, H. 2014. Male accessory gland secretions modulate female post-mating behavior in the moth Spodoptera litura. Journal of Insect Behavior, 27: 105116.CrossRefGoogle Scholar