Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T23:40:59.975Z Has data issue: false hasContentIssue false
  • English
  • Français

Mother-derived trans-generational immune priming in the red palm weevil, Rhynchophorus ferrugineus Olivier (Coleoptera, Dryophthoridae)

Published online by Cambridge University Press:  11 September 2014

Z. H. Shi ,
Y. T. Lin  and
Y. M. Hou
Z. H. Shi
Affiliation:
Key Laboratory of Integrated Pest Management of Fujian-Taiwan Crops, Ministry of Agriculture, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, China
Y. T. Lin
Affiliation:
Key Laboratory of Integrated Pest Management of Fujian-Taiwan Crops, Ministry of Agriculture, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, China
Y. M. Hou*
Affiliation:
Key Laboratory of Integrated Pest Management of Fujian-Taiwan Crops, Ministry of Agriculture, China Fujian Provincial Key Laboratory of Insect Ecology, College of Plant Protection, Fujian Agriculture and Forestry University, China
*
*Author for correspondence Phone: +86-591-83789214 Fax: +86-591-83789214 E-mail: ymhou@fafu.edu.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Rhynchophorus ferrugineus (Coleoptera, Curculionidae) is the most destructive pest of palm trees worldwide containing it invasive areas, such as the southern part of China. It is always emphasized to develop integrated pest management based on biological agents, but their success is not very exciting. Presently, the immune defenses of this pest against biological agents attract scarce attention. It is still unclear whether immune priming also generally occurs in insect pests and in response to different pathogens. Our results indicated that previous challenge of bacteria pathogen enhanced the magnitude of phenoloxidase activity and antibacterial activity in R. ferrugineus larvae against the secondary infection. Furthermore, trans-generational immune priming was also determined in this pest, and only challenged R. ferrugineus mothers transferred the immune protection to their offspring which suggested males and females of this pest might have evolved different strategies on the investment of delivering immune protection to their offspring. Importantly, our data provide the evidence to suggest that different kinds of biological control agents might be used alternatively or in combination to fight against R. ferrugineus because of the existence of immune priming with low species-specific level. On the other hand, for this invasive pest, the immune priming may also facilitate its adaptation and dispersal in the new regions.

Keywords

red palm weevilinsect immunitytrans-generationalantibacterial activity
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 104 , Issue 6 , December 2014 , pp. 742 - 750
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bunerjee, A. & Dangar, T.K. (1995) Pseudomonas aeruginosa, a facultative pathogen of red palm weevil, Rhynchophorus ferrugineus . World Journal of Microbiology and Biotechnology 11, 618–620.Google Scholar
Cerenius, L., Lee, B.L. & Söderhäll, K. (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29, 263–271.Google Scholar
Cherry, S. & Silverman, N. (2006) Host–pathogen interactions in Drosophila: new tricks from an old friend. Nature Immunology 7, 911–917.Google Scholar
Dembilio, ó., Quesada-Moraga, E., Santago-Ālvarez, C. & Jacas, J.A. (2010) Potential of an indigenous strain of the entomopathogenic fungus Beauveria bassiana as a biological control agent against the red palm weevil Rhynchophorus ferrugineus . Journal of Invertebrate Pathology 104, 214–221.Google Scholar
El-Sufty, R., Al-Awash, S.A., Al Amiri, A.M., Shahdad, A.S., Al Bathra, A.H. & Musa, S.A. (2007) Biological control of red palm weevil, Rhynchophorus ferrugineus by the entomopathogenic fungus Beauveria bassiana in United Arab Emirates. Acta Horticulture 736, 399–404.Google Scholar
El-Sufty, R., Al-Awash, S.A., Al-Bgham, S., Shahdad, A.S. & Al-Bathra, A.H. (2009) Pathogenicity of the fungus Beauveria bassiana (Bals.) Vuill to the red palm weevil, Rhynchophorus ferrugineus (Oliv.) (Col: Curculionidae) under laboratory and field conditions. Egyptian Journal of Biological Pest Control 19, 81–85.Google Scholar
EPPO (European, Mediterranean Plant Protection Organization). (2008) Data sheets on quarantine pests-Rhynchophorus ferrugineus . EPPO Bulletin 38, 55–59.Google Scholar
Freitak, D., Schmidtberg, H., Dickel, F., Lochnit, G., Vogel, H. & Vilcinskas, A. (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5, 547–554.Google Scholar
Kaneko, T., Yano, T., Aggarwal, K., Lim, J.H., Ueda, K., Oshima, Y., Peach, C., Erturk-Hasdemir, D., Goldman, W.E., Oh, B., Kurata, S. & Silverman, N. (2006) PGRP-LC and PGRP-LE have essential yet distinct functions in the drosophila immune response to monomeric DAP-type peptidoglycan. Nature Immunology 7, 715–723.Google Scholar
Krawetz, S.A. (2005) Parental contribution: new insights and future challenges. Nature Reviews Genetics 6, 633–642.Google Scholar
Kurtz, J. (2005) Specific memory within innate immune systems. Trends in Immunology 26, 186–192.Google Scholar
Kurtz, J. & Franz, K. (2003) Evidence for memory in invertebrate immunity. Nature 425, 37–38.Google Scholar
Ju, R.T., Li, Y.Z., Du, Y.Z., Chi, X.Z., Yan, W. & Xu, Y. (2006) Alert to spread of an invasive alien species, red palm weevil, Rhynchophorus feerugineus . Chinese Bulletin of Entomology 43, 159–163. (in Chinese with English abstract)Google Scholar
Little, T.J., O'Connor, B., Colegrave, N., Watt, K. & Read, A.F. (2003) Maternal transfer of strain-specific immunity in an invertebrate. Current Biology 13, 489–492.Google Scholar
Little, T.J. & Kraaijeveld, A.R. (2004) Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology and Evolution 19, 58–60.Google Scholar
Llácer, E., Negre, M. & Jacas, J.A. (2012 a) Evaluation of an oil dispersion formulation of imidacloprid as a drench against Rhynchophorus feerugineus in young palm trees. Pest Management Sciences 68, 878–882.Google Scholar
Llácer, E., Santiago-Álvarez, C. & Jacas, J.A. (2012 b) Could sterile males be used to vector a microbiological control agent? The case of Rhynchophorus feerugineus and Beauveria bassiana . Bulletin of Entomological Research 103, 241–250.CrossRefGoogle ScholarPubMed
Manachini, B., Arizza, V., Parrinello, D. & Parrinello, N. (2011) Hemocytes of Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae) and their response to Saccharomyces cerevisiae and Bacillus thuringiensis. Journal of Invertebrate Pathology 106, 360–365.Google Scholar
Moret, Y. & Schmid-Hempel, P. (2001) Immune defence in bumble-bee offspring. Nature 414, 506.Google Scholar
Moore, T. & Haig, D. (1991) Genomic imprinting in mammalian development – a parental tug-of-war. Trends in Genetics 7, 45–49.Google Scholar
Parmakelis, A., Slotman, M.A., Marshall, J.C., Awono-Ambene, P.H., Nkondjio, C.A., Simard, F., Caccone, S. & Powell, J. (2008) The molecular evolution of four antimalarial immune genes in the Anopheles gambiae species complex. BMC Evolutionary Biology 8, 68–79.Google Scholar
Pham, L.N., Dionne, M.S., Shirasu-Hiza, M. & Schneider, D.S. (2007) A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Pathogens 3, e26.Google Scholar
Poorjavad, N., Goldansaz, S.H. & Avand-Faghig, A. (2009) Response of the red palm weevil Rhynchophorus feerugineus to its aggregation pheromone under laboratory conditions. Bulletin of Insectology 62, 257–260.Google Scholar
Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R. & Barilla-Mury, C. (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329, 1353–1355.Google Scholar
Roth, O. & Kurtz, J. (2009) Phagocytosis mediates specificity in the immune defence of an invertebrate, the woodlouse Porcellio scaber (Crustacea: Isopoda). Developmental and Comparative Immunology 33, 1151–1155.CrossRefGoogle ScholarPubMed
Roth, O., Sadd, B.M., Schmid-Hempel, P. & Kurtz, J. (2009) Strain-specific priming of resistance in the red flour beetle, Tribolium castaneum . Proceedings of the Royal Society of London Series B 276, 145–151.Google Scholar
Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P. & Kurtz, J. (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum . Journal of Animal Ecology 79, 403–413.Google Scholar
Sadd, B.M., Schmid-Hempel, P. (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology 16, 1206–1210.CrossRefGoogle ScholarPubMed
Salama, H.S., Foda, M.S., El-Bendary, M.A. & Abdel-Razek, A. (2004) Infection of red palm weevil, Rhynchophorus ferrugineus, by spore-forming bacilli indigenous to its natural habitat in Egypt. Journal of Pest Science 77, 27–31.Google Scholar
Schmid-Hempel, P. (2005) Natural insect host–parasite systems show immune priming and specificity: puzzles to be solved. Bioessays 27, 1026–1034.Google Scholar
Shi, Z.H. & Sun, J.H. (2010) Immunocompetence of the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae, Scolytinae): variation between developmental stages and sexes in populations in China. Journal of Insect Physiology 56, 1696–1701.CrossRefGoogle ScholarPubMed
Siva-Jothy, M.T., Moret, Y., Rolff, J. & Simpson, S.J. (2005) Insect immunity: an evolutionary ecology perspective. Advances in Insect Physiology 32, 1–48.Google Scholar
Trauer, U. & Hilker, M. (2013) Parental legacy in insects: variation of transgenerational immune priming during offspring development. PLoS ONE 8, e63392.Google Scholar
Yue, F., Zhou, Z., Wang, L.L., Ma, Z.P., Wang, J.J., Wang, M.Q., Zhang, H. & Song, L.S. (2013) Maternal transfer of immunity in scallop Chlamys farreri and its trans-generational immune protection to offspring against bacterial challenge. Developmental and Comparative Immunology 41, 569–577.Google Scholar
Zanchi, C., Troussard, J., Martinaud, G., Moreau, J. & Moret, Y. (2011) Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect. Journal of Animal Ecology 80, 1174–1183.Google Scholar