Skip to main content
×
Home
    • Aa
    • Aa

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

  • S. Musmeci (a1), S. Belvedere (a2), R. Sasso (a1), S. Arnone (a1), M. Cristofaro (a1), P. Nobili (a1), A. La Marca (a3) and A. De Biase (a2)...
Abstract
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.

Copyright
Corresponding author
*Author for correspondence Tel.: +39-06.4991.4744 Fax: +39-06.4958.259 E-mail: alessio.debiase@uniroma1.it
References
Hide All
Abdel-AzimM.M., VidyasagarP.S.P.V., AldosariS.A. & MumtazR. (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, 520528.
Al-AyedhH.Y. & RasoolK.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, 157162.
ArnoneS., MusmeciS., CatarciS., SassoR., NobiliP. & CristofaroM. (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.
BaccaroS., CeciliaA. & PasqualiA. (2005) Irradiation Facility at ENEA-CASACCIA Centre (Rome) ENEA: ENEA Report RT/2005/28/FIS 29 pp.
BarclayH.J. (2005) Mathematical models for the use of sterile insects. pp. 147174 in DickV.A., HendrichsJ. & RobinsonA.S. (Eds) Sterile Insect Technique Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.
BelvedereS., La MarcaA., MarcariV., SeniaG. & De BiaseA. (2014) In silico mining of microsatellite markers for the Red Palm Weevil as contribution to its invasion management. Conservation Genetics Resources 6, 947948.
BenjaminiY. & HochbergY. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B57, 289300.
BoormanE. & ParkerG.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, 145155.
ConnerJ.K. (1995) Extreme variability in sperm precedence in the fungus beetle, Bolitotherus cornutus (Coleoptera Tenebrionidae). Ethology Ecology & Evolution 7, 277280.
CookP.A., HarveyI.F. & ParkerG.A. (1997) Predicting variation in sperm precedence. Philosophical Transactions of the Royal Society B, 352, 771780.
CristofaroM., SassoR., MusmeciS., ArnoneS., Di IlioV., De BiaseA. & BelvedereS. (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.
DanielssonI. (1998) Mechanisms of sperm competition in insects. Annales Zoologici Fennici 35, 241257.
DembilioÓ. & JacasJ.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, 153163.
El-MergawyR.A.A.M. & Al-AjlanA.M. (2011) Red palm weevil, Rhynchophorus ferrugineus (Olivier): economic importance, biology, biogeography and integrated pest management. Journal of Agricultural Science and Technology A 1, 123.
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.
Esteban-DurànJ., YelaJ.L., CrespoF.B. & AlvarezA.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, 737748.
FaghihA.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, 1618.
FaleiroJ.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, 135154.
FAO (2005) Provisional Additions, Glossary of Phytosanitary Terms. Rome, Italty, Secretariat of the International Plant Protection Convention (IPPC), FAO.
GothiK.K., HireR.S., VijayalakshmiN. & DongreT.K. (2007) Studies on mating behaviour of radio-sterilized males of Red Palm Weevil, Rhynchophorus ferrugineus Olivier. Journal of Nuclear Agriculture and Biology 36, 6572.
GwynneD.T. (1984) Male mating effort, confidence of paternity, and insect sperm competition. pp. 117149 in SmithR.L. (Ed.) Sperm Competition and the Evolution of Animal Mating Systems. New York, Academic Press Inc.
HaranoT., NakamotoY. & MiyatakeT. (2008) Sperm precedence in Callosobruchus chinensis estimated using the sterile male technique. Journal of Ethology 26, 201206.
HarariA.R., LandoltP.J., O'BrienC.W. & BrockmannH.J. (2003) Prolonged mate guarding and sperm competition in the weevil Diaprepes abbreviatus (L.). Behavioral Ecology 14, 8996.
HendrichsJ.H., RobinsonA.S., CayolJ.P. & EnkerlinW. (2002) Medfly Area-Wide Sterile Insect Technique programmes for prevention, suppression or eradication: the importance of mating behavior studies. Florida Entomologist 85, 113.
InceS., PorcelliF. & Al-JbooryI. (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, 13681374.
InghilesiA., MazzaG., CiniA. & CervoR. (2014) Comportamento sociale e riproduttivo del punteruolo rosso delle palme: approfondire le conoscenze per contrastare questo flagello. Atti Accademia Nazionale Italiana di Entomologia 61, 189192.
InghilesiA., MazzaG., CervoR. & CiniA. (2015) A network of sex and competition: the promiscuous mating system of an invasive weevil. Current Zoology 61, 8597.
JuR.T., WangF., WanF.H. & LiB. (2011) Effect of host plants on development and reproduction of Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae). Journal of Pest Science 84, 3339.
KaakehW. (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, 2333.
KehatM. (1999) Threat to date palms in Israel, Jordan and Palestian authority by the Red Palm Weevil, Rhynchophorus ferrugineus . Phytoparasitica 27, 241242.
KlassenW. (2005) Area-wide integrated pest management and the Sterile Insect Technique. pp. 3968 in DyckV.A., HendrichsJ. & RobinsonA.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.
KniplingE.F. (1955) Possibilities of insect control or eradication through the use of sexually sterile males. Journal of Economic Entomology 48, 459462.
KniplingE.F. (1968) The potential role of sterility for pest control. pp. 740 in LaBrecqueG.C. & SmithC.N. (Eds) Principles of Insect Chemosterilization. New York, USA, Appleton-Century-Crofts.
KrishnakumarR. & MaheshwariP. (2007) Assessment of the Sterile Insect Technique to manage Red Palm Weevil Rhynchophorus ferrugineus in coconut. pp. 475485 in VreysenM.J.B., RobinsonA.S. & HendrichsJ. (Eds) Area-Wide Control of Insect Pests. The Netherlands, Springer.
LanceD.R. & McInnisD.O. (2005) Biological Basis of the Sterile Insect Technique. pp. 6994 in DyckV.A., HendrichsJ. & RobinsonA.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.
LeeS.G., McCombsS.D. & SaulS.H. (2003) Sperm precedence of irradiated Mediterranean fruit fly males (Diptera: Tephritidae). Proceedings of Hawaiian Entomological Society 36, 4759.
LewisS.M. & AustadS.N. (1990) Sources of intraspecific variation in sperm precedence in red flour beetles. The American Naturalist 135, 351359.
LlácerE., Santiago-ÁlvarezC. & JacasJ.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, 241250.
MazzaG., FrancardiV., InghilesiA.F., StasollaG., BenvenutiC., CiniA., BarzantiG.P., CitoA., ArnoneS., CristofaroM., MusmeciS., SassoR., CamerotaM., CervoR. & RoversiP.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.
MazzaG., InghilesiA.F., StasollaG., CiniA., CervoR., BenvenutiC., FrancardiV., CristofaroM., ArnoneS. & RoversiP.F. (2016) Sterile Rhynchophorus ferrugineus males efficiently impair reproduction while maintaining their sexual competitiveness in a social context. Journal of Pest Science 89, 459468.
MurphyS.T. & BriscoeB.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, 3546.
MusmeciS., CristofaroM., ArnoneS., SassoR., BaccaroS., PasqualiA. & CatarciS. (2013) Controllo del punteruolo rosso mediante la tecnica del maschio sterile (SIT): utopia o realtà? Atti Accademia Nazionale Italiana di Entomologia 61, 239246.
PaoliF., DallaiR., CristofaroM., ArnoneS., FrancardiV. & RoversiP.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, 274285.
PrabhuS.T. & PatilR.S. (2010) Studies on the biological aspects of red palm weevil, Rhynchophorus ferrugineus (Oliv.). Karnataka Journal of Agricultural Sciences 22, 732733.
PrabhuS.T., DongreT.K. & PatilR.S. (2010) Effect of irradiation on the biological activities of red palm weevil, Rhynchophorus ferrugineus Olivier. Karnataka Journal of Agricultural Sciences 23, 186188.
RahalkarG.W., HarwalkarM.R., RananavareH.D., ShantaramK. & AyengarA.R.G. (1973) Laboratory studies on radiation sterilization of Rhynchophorus ferrugineus males. Journal of Plantation Crops 1, 141145.
RahalkarG.W., HarwalkarM.R. & RananavareH.D. (1975) Laboratory studies on sterilization of male Rhynchophorus ferrugineus . pp. 261267 in Sterility Principle for Insect Control 1974. Vienna, Austria, International Atomic Energy Agency (Ed.).
RahalkarG.W., HarwalkarM.R., RananvareH.D., KurianC., AbrhamV.A. & KoyaK.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, 6568.
RamachandranC.P. (1991) Effect of gamma radiation on various stages of red date palm weevil, Rhynchophorus ferrugineus Oliv. Journal of Nuclear Agriculture and Biology 3, 218221.
RobinsonA.S. & HendrichsJ. (2005) Prospects for the future development and application of the sterile insect technique. pp. 727760 in DyckV.A., HendrichsJ. & RobinsonA.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.
Rugman-JonesP.F., HoddleC.D., HoddleM.S. & StouthamerR. (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.
ScolariF., YuvalB., GomulskiL.M., ScheteligM. F., GabrieliP., BassettiF., WimmerE.A., MalacridaA.R. & GasperiG. (2014) Polyandry in the medfly – shifts in paternity mediated by sperm stratification and mixing. BMC Genetics 15(Suppl. 2), S10, 18. doi: 10.1186/1471-2156-15-S2-S10.
Sillen-TullbergB. (1981) Prolonged copulation: a male ‘postcopulatory’ strategy in a promiscuous species, Lygaeus equestris (Heteroptera: Lygaeidae). Behavioral Ecology and Sociobiology 9, 283289.
SimmonsL.W. (2001) Sperm Competition and its Evolutionary Consequences in the Insects. Princeton, New Jersey, USA, Princeton University Press (Ed.).
SPSS Inc. Released (2008) SPSS Statistics for Windows, Version 17.0. Chicago: SPSS Inc.
SquiresZ.E., WongB., NormanM.D. & Stuart-FoxD. (2015) Last male sperm precedence in a polygamous squid. Biological Journal of the Linnean Society 116(2), 277287.
WhittenM. & MahonR. (2005) Misconception and constraints. pp. 601626 in DyckV.A., HendrichsJ. & RobinsonA.S. (Eds) Sterile Insect Technique: Principles and Practice in Area-Wide Integrated Pest Management. The Netherlands, Springer.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Bulletin of Entomological Research
  • ISSN: 0007-4853
  • EISSN: 1475-2670
  • URL: /core/journals/bulletin-of-entomological-research
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 6 *
Loading metrics...

Abstract views

Total abstract views: 90 *
Loading metrics...

* Views captured on Cambridge Core between 3rd October 2017 - 19th October 2017. This data will be updated every 24 hours.