Eur. J. Entomol. 113: 309-314, 2016 | 10.14411/eje.2016.039

Reproductive status of Tribolium castaneum (Coleoptera: Tenebrionidae) affects its response to infection by Steinernema feltiae (Rhabditida: Steinernematidae)

Paulina KRAMARZ1, Dariusz MA£EK1, Maria GAWE£1, Szymon M. DROBNIAK1, Joanna HOMA2
1 Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland; e-mails: paulina.kramarz@uj.edu.pl, dariusz.malek@uj.edu.pl, maria.gawel@uj.edu.pl, szymek.drobniak@uj.edu.pl
2 Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland; e-mail: joanna.homa@uj.edu.pl

Gender-specific reproductive roles are important factors determining sexual dimorphism. Here, we investigate the effects of sex-based differences and reproductive status on the defence of Tribolium castaneum (Herbst, 1797) (Coleoptera: Tenebrionidae) against infection by Steinernema feltiae (Filipjev, 1934) (Rhabditida: Steinernematidae). Female and male beetles, either virgin or post-copulation, were exposed individually to nematodes. Individuals were then sampled every 12 h, dissected, and checked for the presence of nematodes; we also measured their phenoloxidase (PO) activity. Reproductive status affected resistance to nematodes and PO activity as infected virgin individuals had a higher PO activity and lower mortality than reproducing individuals, with no differences between sexes. Mortality also increased with time, while PO activity did not change. Parasite load was related to reproductive status and sex, with reproducing females with the highest parasite loads in all treatments, and virgin males with more nematodes than sexually active males. Our results indicate that the costs of reproduction impair the immunological system of T. castaneum similarly in both sexes. It is possible, however, that other components of the immunological system that we did not measure, such as lysozyme activity, are impaired by infection with S. feltiae in a sex-specific way.

Keywords: Coleoptera, Tenebrionide, Tribolium castaneum, Rhabditida, Steinernematidae, Steinernema feltiae, phenoloxidase, sexual dimorphism, infection

Received: November 25, 2015; Accepted: March 14, 2016; Published online: April 5, 2016

Download citation

References

  1. Adamo S.A., Jensen M. & Younger M. 2001: Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. - Anim. Behav. 62: 417-425. Go to original source...
  2. Alexander J. & Stimson W.H. 1988: Sex hormones and the course of parasite infection. - Parasitol. Today 4: 189-193. Go to original source...
  3. Bateman A.J. 1948: Intra-sexual selection in Drosophila. - Heredity 2: 349-368. Go to original source...
  4. Bathon H. 1996: Impact of entomopathogenic nematodes on non-target hosts. - Biocontr. Sci. Techn. 6: 421-434. Go to original source...
  5. Bucher G. 2009: The Beetle Book. Published online by the author. URL: www.gwdg.de/~gbucher1/tribolium-castaneum-beetle-book1.pdf.
  6. Cichoñ M. 1997: Evolution of longevity through optimal resource allocation. - Proc. R. Soc. Lond. (B) 264: 1383-1388. Go to original source...
  7. Cerenius L., Lee B.L. & Söderhäll K. 2008: The proPO-system: pros and cons for its role in invertebrate immunity. - Trends Immunol. 29: 263-271. Go to original source...
  8. Córdoba-Aguilar A. & Munguía-Steyer R. 2013: The sicker sex: understanding male biases in parasitic infection, resource allocation and fitness. - PLoS One 8(3): e76246, 7 pp. Go to original source...
  9. Córdoba-Aguilar A., Ruiz-Silva D., Munguía-Steyer R. & Lanz-Mendoza H. 2011: Do reproductive activities compromise immunological competence as measured by phenoloxidase activity? Field and experimental manipulation in females of two damselfly species. - Physiol. Entomol. 36: 335-342. Go to original source...
  10. Cotter S.C., Kruuk L.E.B. & Wilson K. 2004: Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. - J. Evol. Biol. 172: 421-429.
  11. Freitak D., Knorr E., Vogel H. & Vilcinskas A. 2012: Gender- and microRNA expression in Tribolium castaneum. - Biol. Lett. 8: 860-863. Go to original source...
  12. French S.S., De Nardo D.F. & Moore M.C. 2007: Trade-offs between the reproductive and immune systems: facultative responses to resources or obligate responses to reproduction? - Am. Nat. 170: 79-89. Go to original source...
  13. Georgis R., Koppenhofer A.M., Lacey L.A., Bélair G., Duncan L.W., Grewal P.S., Samish M., Tan L., Torr P. & van Tol R.W.H.M. 2006: Successes and failures in the use of parasitic nematodes for pest control. - Biol. Contr. 38: 103-123. Go to original source...
  14. Gillespie J.P., Kanost M.R. & Trenczek T. 1997: Biological mediators of insect immunity. - Annu. Rev. Entomol. 42: 611-643. Go to original source...
  15. González-Santoyo I. & Córdoba-Aguilar A. 2012: Phenoloxidase: a key component of the insect immune system. - Entomol. Exp. Appl. 142: 1-16. Go to original source...
  16. Gray D.A. 1998: Sex differences in susceptibility of house crickets, Acheta domesticus, to experimental infection with Serratia liquefaciens. - J. Invertebr. Pathol. 71: 288-289. Go to original source...
  17. Hirao A., Ehlers R.-U. & Strauch O. 2010: Life cycle and population development of the entomopathogenic nematodes Steinernema carpocapsae and S. feltiae (Nematoda, Rhabditida) in monoxenic liquid culture. - Nematology 12: 201-210. Go to original source...
  18. Kraaijeveld A. & Godfray H. 1997: Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. - Nature 389: 278-280. Go to original source...
  19. Lavine M.D. & Strand M.R. 2002: Insect haemocytes and their role in immunity. - Insect Biochem. Mol. Biol. 32: 1295-1309. Go to original source...
  20. Milutinoviæ B., Stolpe C., Peuβ R., Armitage S.A. & Kurtz J. 2013: The red flour beetle as a model for bacterial oral infections. - PloS One 8(5): e64638, 12 pp. Go to original source...
  21. Moore S.L. & Wilson K. 2002: Parasites as a viability cost of sexual selection in natural populations of mammals. - Science 297: 2015-2018. Go to original source...
  22. Nava-Sánchez A., González-Tokman D., Munguía-Steyer R. & Córdoba-Aguilar A. 2015: Does mating activity impair phagocytosis-mediated priming immune response? A test using the house cricket, Acheta domesticus. - Acta Ethol. 18: 295-299. Go to original source...
  23. Nunn C.L., Lindenfors P., Pursall E.R. & Rolff J. 2009: On sexual dimorphism in immune function. - Philos. Trans. R. Soc. Lond. (B) 364: 61-69. Go to original source...
  24. Perrin N. & Sibly R. 1993: Dynamic models of energy allocation and investment. - Annu. Rev. Ecol. Syst. 24: 379-410. Go to original source...
  25. Poulin R. 1996: Sexual inequalities in helminth infections: a cost of being a male? - Am. Nat. 147: 287-295. Go to original source...
  26. R Development Core Team 2012: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
  27. Ramos-Rodríguez O., Campbell J.F. & Ramaswamy S.B. 2006: Pathogenicity of three species of entomopathogenic nematodes to some major stored-product insect pests. - J. Stor. Prod. Res. 42: 241-252. Go to original source...
  28. Rolff J. 2002: Bateman's principle and immunity. - Proc. R. Soc. (B) 269: 867-872. Go to original source...
  29. Rolff J. & Siva-Jothy M.T. 2002: Copulation corrupts immunity: a mechanism for a cost of mating in insects. - Proc. Natl. Acad. Sci. U.S.A. 99: 9916-9918. Go to original source...
  30. Rossi E., Cosimi S. & Loni A. 2010: Insecticide resistance in Italian populations of Tribolium flour beetles. - Bull. Insectol. 63: 251-258.
  31. Scharf I., Peter F. & Martin O.Y. 2012: Reproductive trade-offs and direct costs for males in arthropods. - Evol. Biol. 40: 169-184. Go to original source...
  32. Schmid-Hempel P. 2011: Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology, and Genetics. Oxford University Press, New York, 544 pp.
  33. Schmid-Hempel P. & Ebert D. 2003: On the evolutionary ecology of specific immune defence. - Trends Ecol. Evol. 18: 27-32. Go to original source...
  34. Schwarzenbach G.A., Hosken D.J. & Ward P.I. 2005: Sex and immunity in the yellow dung fly Scathophaga stercoraria. - J. Evol. Biol. 18: 455-463. Go to original source...
  35. Siva-Jothy M.T., Tsubaki Y. & Hooper R.E. 1998: Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. - Physiol. Entomol. 23: 274-277. Go to original source...
  36. Siva-Jothy M.T., Tsubaki Y., Hooper R.E. & Plaistow S.J. 2001: Investment in immune function under chronic and acute immune challenge in an insect. - Physiol. Entomol. 26: 1-5. Go to original source...
  37. Sokoloff A. 1974: The Biology of Tribolium, with Special Emphasis on Genetic Aspects. Vol. 2. Clarendon Press, Oxford, 610 pp.
  38. Stoehr A.M. & Kokko H. 2006: Sexual dimorphism in immunocompetence: what does life-history theory predict? - Behav. Ecol. 17: 751-756. Go to original source...
  39. Wedekind C. & Jakobsen P.J. 1998: Male-biased susceptibility to helminth infection: an experimental test with a copepod. - Oikos 81: 458-462. Go to original source...
  40. Zuk M. 1990: Reproductive strategies and disease susceptibility: an evolutionary viewpoint. - Parasitol. Today 6: 231-233. Go to original source...
  41. Zuk M. & McKean K.A. 1996: Sex differences in parasite infections: patterns and processes. - Int. J. Parasitol. 26: 1009-1024. Go to original source...