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Last-male sperm precedence in Rhynchophorus ferrugineus (Olivier): observations in laboratory mating experiments with irradiated males

Published online by Cambridge University Press:  03 October 2017

S. Musmeci ,
S. Belvedere ,
R. Sasso ,
S. Arnone ,
M. Cristofaro ,
P. Nobili ,
A. La Marca  and
A. De Biase
S. Musmeci
Affiliation:
ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
S. Belvedere
Affiliation:
Department of Biology and Biotechnology ‘Charles Darwin’, Sapienza Rome University, Viale dell'Università 32, 00185 Rome, Italy
R. Sasso
Affiliation:
ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
S. Arnone
Affiliation:
ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
M. Cristofaro
Affiliation:
ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
P. Nobili
Affiliation:
ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
A. La Marca
Affiliation:
BBCA-onlus, Via Angelo Signorelli 105, 00123 Rome, Italy
A. De Biase*
Affiliation:
Department of Biology and Biotechnology ‘Charles Darwin’, Sapienza Rome University, Viale dell'Università 32, 00185 Rome, Italy
*
*Author for correspondence Tel.: +39-06.4991.4744 Fax: +39-06.4958.259 E-mail: [email protected]
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Abstract

The Red Palm Weevil (RPW) Rhynchophorus ferrugineus (Olivier 1790) is an invasive pest from southeastern Asia and Melanesia that in the last 30 years has spread widely in the Middle East and Mediterranean Basin. Its stem-boring larvae cause great damage to several palm species of the Arecaceae family, many of which are economically important for agricultural and ornamental purposes. Therefore, great attention has recently been focused in studying this species to identify sustainable and effective eradication strategies, such as sterile insect technique (SIT). The rapid spread of RPW is associated with its high reproductive success. To evaluate the suitability of a SIT strategy, particular physiological and behavioral aspects of RPW reproduction, such as the presence of polyandry and post-copulatory sperm selection mechanisms, were investigated. To determine paternity of progeny from multiply mated females, double-crossing experiments were carried out confining individual females with either a wild-type male or a γ-irradiated male (Co-60). Fecundity and fertility of females were scored to evaluate post-copulatory sperm selection. Results showed that progeny were almost exclusively produced by the sperm of the second male, suggesting that a last-male sperm precedence is expressed at high levels in this species, and providing interesting insights for an area-wide RPW management strategy such as the SIT.

Keywords

last-male sperm precedencepaternity assignmentsterile insect techniqueRed Palm Weevil
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 1 , February 2018 , pp. 93 - 100
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Copyright
Copyright © Cambridge University Press 2017 

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References

Abdel-Azim, M.M., Vidyasagar, P.S.P.V., Aldosari, S.A. & Mumtaz, R. (2012) Impact of mating frequency on fecundity, fertility and longevity of red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Journal of Agricultural Science and Technology A 2, 520–528.Google Scholar
Al-Ayedh, H.Y. & Rasool, K.G. (2010) Sex ratio and the role of mild relative humidity in mating behaviour of red date palm weevil Rhynchophorus ferrugineus Oliv. (Coleoptera: Curculionidae) gamma-irradiated adults. Journal of Applied Entomology 134, 157–162.CrossRefGoogle Scholar
Arnone, S., Musmeci, S., Catarci, S., Sasso, R., Nobili, P. & Cristofaro, M. (2014) Allevamento del punteruolo rosso delle palme: un contributo per la sperimentazione in campo e per studi di laboratorio. p. 107 in XXIV Italian Congress of Entomology, 9–14 June 2014, Orosei (NU), Società Entomologica Italiana.Google Scholar
Baccaro, S., Cecilia, A. & Pasquali, A. (2005) Irradiation Facility at ENEA-CASACCIA Centre (Rome) ENEA: ENEA Report RT/2005/28/FIS 29 pp.Google Scholar
Barclay, H.J. (2005) Mathematical models for the use of sterile insects. pp. 147–174 in Dick, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.CrossRefGoogle Scholar
Belvedere, S., La Marca, A., Marcari, V., Senia, G. & De Biase, A. (2014) In silico mining of microsatellite markers for the Red Palm Weevil as contribution to its invasion management. Conservation Genetics Resources 6, 947–948.CrossRefGoogle Scholar
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B57, 289–300.Google Scholar
Boorman, E. & Parker, G.A. (1976) Sperm (ejaculate) competition in Drosophila melanogaster, and the reproductive value of females to males in relation to female age and mating status. Ecological Entomology 1, 145–155.CrossRefGoogle Scholar
Conner, J.K. (1995) Extreme variability in sperm precedence in the fungus beetle, Bolitotherus cornutus (Coleoptera Tenebrionidae). Ethology Ecology & Evolution 7, 277–280.CrossRefGoogle Scholar
Cook, P.A., Harvey, I.F. & Parker, G.A. (1997) Predicting variation in sperm precedence. Philosophical Transactions of the Royal Society B, 352, 771–780.CrossRefGoogle Scholar
Cristofaro, M., Sasso, R., Musmeci, S., Arnone, S., Di Ilio, V., De Biase, A. & Belvedere, S. (2011) Primi risultati relativi ad uno studio di fattibilità della tecnica dell’insetto sterile per il controllo di. Rhynchophorus ferrugineus Olivier. p. 292 in XXIII Italian Congress of Entomology, 13–16 June 2011, Genova, Società Entomologica Italiana.Google Scholar
Danielsson, I. (1998) Mechanisms of sperm competition in insects. Annales Zoologici Fennici 35, 241–257.Google Scholar
Dembilio, Ó. & Jacas, J.A. (2011) Basic bio-ecological parameters of the invasive Red Palm Weevil, Rhynchophorus ferrugineus (Coleoptera: Curculionidae), in Phoenix canariensis under Mediterranean climate. Bulletin of Entomological Research 101, 153–163.CrossRefGoogle ScholarPubMed
El-Mergawy, R.A.A.M. & Al-Ajlan, A.M. (2011) Red palm weevil, Rhynchophorus ferrugineus (Olivier): economic importance, biology, biogeography and integrated pest management. Journal of Agricultural Science and Technology A 1, 1–23.Google Scholar
EPPO Standards (2015) A1 and A2 lists of pests recommended for regulation as quarantine pests. European and Mediterranean Plant Protection Organization. 21 Boulevard Richard Lenoir, 75011 Paris, France, September 2015. https://www.eppo.int/QUARANTINE/listA2.htm.Google Scholar
Esteban-Duràn, J., Yela, J.L., Crespo, F.B. & Alvarez, A.J. (1998) Biology of red palm weevil, Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae: Rhynchophorinae), in the laboratory and field life cycle, biological characteristics in its zone of introduction in Spain, biological method of detection and possible control. Boletin de Sanidad Vegetal Plagas 24, 737–748.Google Scholar
Faghih, A.A. (1996) The biology of red palm weevil, Rhynchophorus ferrugineus Oliv. (Coleoptera, Curculionidae) in Saravan region (Sistan & Balouchistan province, Iran). Applied Entomology and Phytopathology 63, 16–18.Google Scholar
Faleiro, J.R. (2006) A review of the issues and management of the red palm weevil Rhynchophorus ferrugineus (Coleoptera: Rhynchophoridae) in coconut and date palm during the last one hundred years. International Journal of Tropical Insect Science 26, 135–154.Google Scholar
FAO (2005) Provisional Additions, Glossary of Phytosanitary Terms. Rome, Italty, Secretariat of the International Plant Protection Convention (IPPC), FAO.Google Scholar
Gothi, K.K., Hire, R.S., Vijayalakshmi, N. & Dongre, T.K. (2007) Studies on mating behaviour of radio-sterilized males of Red Palm Weevil, Rhynchophorus ferrugineus Olivier. Journal of Nuclear Agriculture and Biology 36, 65–72.Google Scholar
Gwynne, D.T. (1984) Male mating effort, confidence of paternity, and insect sperm competition. pp. 117–149 in Smith, R.L. (Ed.) Sperm Competition and the Evolution of Animal Mating Systems. New York, Academic Press Inc. CrossRefGoogle Scholar
Harano, T., Nakamoto, Y. & Miyatake, T. (2008) Sperm precedence in Callosobruchus chinensis estimated using the sterile male technique. Journal of Ethology 26, 201–206.CrossRefGoogle Scholar
Harari, A.R., Landolt, P.J., O'Brien, C.W. & Brockmann, H.J. (2003) Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.). Behavioral Ecology 14, 89–96.CrossRefGoogle Scholar
Hendrichs, J.H., Robinson, A.S., Cayol, J.P. & Enkerlin, W. (2002) Medfly Area-Wide Sterile Insect Technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist 85, 1–13.CrossRefGoogle Scholar
Ince, S., Porcelli, F. & Al-Jboory, I. (2011) Egg laying and egg laying behavior of red palm weevil Rhynchophorus ferrugineus (Olivier) 1790 (Coleoptera: Curculionidae). Agriculture and Biology Journal of North America 2, 1368–1374.CrossRefGoogle Scholar
Inghilesi, A., Mazza, G., Cini, A. & Cervo, R. (2014) Comportamento sociale e riproduttivo del punteruolo rosso delle palme: approfondire le conoscenze per contrastare questo flagello. Atti Accademia Nazionale Italiana di Entomologia 61, 189–192.Google Scholar
Inghilesi, A., Mazza, G., Cervo, R. & Cini, A. (2015) A network of sex and competition: the promiscuous mating system of an invasive weevil. Current Zoology 61, 85–97.CrossRefGoogle Scholar
Ju, R.T., Wang, F., Wan, F.H. & Li, B. (2011) Effect of host plants on development and reproduction of Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Journal of Pest Science 84, 33–39.CrossRefGoogle Scholar
Kaakeh, W. (2005) Longevity, fecundity, and fertility of the red palm weevil, Rynchophorus ferrugineus Olivier (Coleoptera: Curculionidae) on natural and artificial diets. Emirates Journal of Agricultural Sciences 17, 23–33.Google Scholar
Kehat, M. (1999) Threat to date palms in Israel, Jordan and Palestian authority by the Red Palm Weevil, Rhynchophorus ferrugineus . Phytoparasitica 27, 241–242.CrossRefGoogle Scholar
Klassen, W. (2005) Area-wide integrated pest management and the Sterile Insect Technique. pp. 39–68 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.CrossRefGoogle Scholar
Knipling, E.F. (1955) Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology 48, 459–462.CrossRefGoogle Scholar
Knipling, E.F. (1968) The potential role of sterility for pest control. pp. 7–40 in LaBrecque, G.C. & Smith, C.N. (Eds) Principles of Insect Chemosterilization. New York, USA, Appleton-Century-Crofts.Google Scholar
Krishnakumar, R. & Maheshwari, P. (2007) Assessment of the Sterile Insect Technique to manage Red Palm Weevil Rhynchophorus ferrugineus in coconut. pp. 475–485 in Vreysen, M.J.B., Robinson, A.S. & Hendrichs, J. (Eds) Area-Wide Control of Insect Pests. The Netherlands, Springer.CrossRefGoogle Scholar
Lance, D.R. & McInnis, D.O. (2005) Biological Basis of the Sterile Insect Technique. pp. 69–94 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.CrossRefGoogle Scholar
Lee, S.G., McCombs, S.D. & Saul, S.H. (2003) Sperm precedence of irradiated Mediterranean fruit fly males (Diptera: Tephritidae). Proceedings of Hawaiian Entomological Society 36, 47–59.Google Scholar
Lewis, S.M. & Austad, S.N. (1990) Sources of intraspecific variation in sperm precedence in red flour beetles. The American Naturalist 135, 351–359.CrossRefGoogle Scholar
Llácer, E., Santiago-Álvarez, C. & Jacas, J.A. (2013) Could sterile males be used to vector a microbiological control agent? The case of Rhynchophorus ferrugineus and Beauveria bassiana . Bulletin of Entomological Research 103, 241–250.CrossRefGoogle ScholarPubMed
Mazza, G., Francardi, V., Inghilesi, A.F., Stasolla, G., Benvenuti, C., Cini, A., Barzanti, G.P., Cito, A., Arnone, S., Cristofaro, M., Musmeci, S., Sasso, R., Camerota, M., Cervo, R. & Roversi, P.F. (2014) Analisi del comportamento sociale e riproduttivo dei maschi sterili di Rhynchophorus ferrugineus: implicazioni per il controllo biologico con agenti entomopatogeni. p. 103 in XXIV Italian Congress of Entomology, 9–14 June 2014 Orosei (NU), Società Entomologica Italiana.Google Scholar
Mazza, G., Inghilesi, A.F., Stasolla, G., Cini, A., Cervo, R., Benvenuti, C., Francardi, V., Cristofaro, M., Arnone, S. & Roversi, P.F. (2016) Sterile Rhynchophorus ferrugineus males efficiently impair reproduction while maintaining their sexual competitiveness in a social context. Journal of Pest Science 89, 459–468.CrossRefGoogle Scholar
Murphy, S.T. & Briscoe, B.R. (1999) The red palm weevil as an alien invasive: biology and the prospects for biological control as a component of IPM. Biocontrol News and Information 20, 35–46.Google Scholar
Musmeci, S., Cristofaro, M., Arnone, S., Sasso, R., Baccaro, S., Pasquali, A. & Catarci, S. (2013) Controllo del punteruolo rosso mediante la tecnica del maschio sterile (SIT): utopia o realtà? Atti Accademia Nazionale Italiana di Entomologia 61, 239–246.Google Scholar
Paoli, F., Dallai, R., Cristofaro, M., Arnone, S., Francardi, V. & Roversi, P.F. (2014) Morphology of the male reproductive system, sperm ultrastructure and γ-irradiation of the red palm weevil Rhynchophorus ferrugineus Oliv. (Coleoptera: Dryophthoridae). Tissue and Cell 46, 274–285.CrossRefGoogle ScholarPubMed
Prabhu, S.T. & Patil, R.S. (2010) Studies on the biological aspects of red palm weevil, Rhynchophorus ferrugineus (Oliv.). Karnataka Journal of Agricultural Sciences 22, 732–733.Google Scholar
Prabhu, S.T., Dongre, T.K. & Patil, R.S. (2010) Effect of irradiation on the biological activities of red palm weevil, Rhynchophorus ferrugineus Olivier. Karnataka Journal of Agricultural Sciences 23, 186–188.Google Scholar
Rahalkar, G.W., Harwalkar, M.R., Rananavare, H.D., Shantaram, K. & Ayengar, A.R.G. (1973) Laboratory studies on radiation sterilization of Rhynchophorus ferrugineus males. Journal of Plantation Crops 1, 141–145.Google Scholar
Rahalkar, G.W., Harwalkar, M.R. & Rananavare, H.D. (1975) Laboratory studies on sterilization of male Rhynchophorus ferrugineus . pp. 261–267 in Sterility Principle for Insect Control 1974. Vienna, Austria, International Atomic Energy Agency (Ed.).Google Scholar
Rahalkar, G.W., Harwalkar, M.R., Rananvare, H.D., Kurian, C., Abrham, V.A. & Koya, K.M.A. (1977) Preliminary field studies on the control of the red palm weevil, Rhynchophorus ferrugineus using radio sterilized males. Journal of Nuclear Agriculture and Biology 6, 65–68.Google Scholar
Ramachandran, C.P. (1991) Effect of gamma radiation on various stages of red date palm weevil, Rhynchophorus ferrugineus Oliv. Journal of Nuclear Agriculture and Biology 3, 218–221.Google Scholar
Robinson, A.S. & Hendrichs, J. (2005) Prospects for the future development and application of the sterile insect technique. pp. 727–760 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.CrossRefGoogle Scholar
Rugman-Jones, P.F., Hoddle, C.D., Hoddle, M.S. & Stouthamer, R. (2013) The lesser of two weevils: molecular-genetics of pest palm weevil populations confirm Rhynchophorus vulneratus (Panzer 1798) as a valid species distinct from R. ferrugineus (Olivier 1790), and reveal the global extent of both. PLoS ONE 8, e78379.CrossRefGoogle Scholar
Scolari, F., Yuval, B., Gomulski, L.M., Schetelig, M. F., Gabrieli, P., Bassetti, F., Wimmer, E.A., Malacrida, A.R. & Gasperi, G. (2014) Polyandry in the medfly – shifts in paternity mediated by sperm stratification and mixing. BMC Genetics 15(Suppl. 2), S10, 1–8. doi: 10.1186/1471-2156-15-S2-S10.Google ScholarPubMed
Sillen-Tullberg, B. (1981) Prolonged copulation: a male ‘postcopulatory’ strategy in a promiscuous species, Lygaeus equestris (Heteroptera: Lygaeidae). Behavioral Ecology and Sociobiology 9, 283–289.CrossRefGoogle Scholar
Simmons, L.W. (2001) Sperm Competition and its Evolutionary Consequences in the Insects. Princeton, New Jersey, USA, Princeton University Press (Ed.).Google Scholar
SPSS Inc. Released (2008) SPSS Statistics for Windows, Version 17.0. Chicago: SPSS Inc.Google Scholar
Squires, Z.E., Wong, B., Norman, M.D. & Stuart-Fox, D. (2015) Last male sperm precedence in a polygamous squid. Biological Journal of the Linnean Society 116(2), 277–287.CrossRefGoogle Scholar
Whitten, M. & Mahon, R. (2005) Misconception and constraints. pp. 601–626 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.CrossRefGoogle Scholar