Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T10:08:50.445Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of inbreeding on potential and realized immune responses in Tenebrio molitor

Published online by Cambridge University Press:  27 April 2011

MARKUS J. RANTALA ,
HEIDI VIITANIEMI  and
DEREK A. ROFF
MARKUS J. RANTALA*
Affiliation:
Department of Biology, Section of Ecology, University of Turku, FIN-20014 Turku, Finland
HEIDI VIITANIEMI
Affiliation:
Department of Biology, Section of Ecology, University of Turku, FIN-20014 Turku, Finland
DEREK A. ROFF
Affiliation:
Department of Biology, University of California, Riverside, CA 92521, USA
*
*Corresponding author: Department of Biology, Section of Ecology, University of Turku, FIN-20014 Turku, Finland. E-mail: markus.rantala@utu.fi
Get access Rights & Permissions [Opens in a new window]

Summary

Although numerous studies on vertebrates suggest that inbreeding reduces their resistance against parasites and pathogens, studies in insects have found contradictory evidence. In this study we tested the effect of 1 generation of brother–sister mating (inbreeding) on potential and realized immune responses and other life-history traits in Tenebrio molitor. We found that inbreeding reduced adult mass, pre-adult survival and increased development time, suggesting that inbreeding reduced the condition of the adults and thus potentially made them more susceptible to physiological stress. However, we found no significant effect of inbreeding on the potential immune response (encapsulation response), but inbreeding reduced the realized immune response (resistance against the entomopathogenic fungi, Beauveria bassiana). There was a significant family effect on encapsulation response, but no family effect on the resistance against the entomopathogenic fungi. Given that this latter trait showed significant inbreeding depression and that the sample size for the family-effect analysis was small it is likely that the lack of a significant family effect is due to reduced statistical power, rather than the lack of a heritable basis to the trait. Our study highlights the importance of using pathogens and parasites in immunoecological studies.

Keywords

encapsulationBeauveria bassianaheterozygosityhomozygosityimmunocompetence
Type
Research Article
Information
Parasitology , Volume 138 , Issue 7 , June 2011 , pp. 906 - 912
Copyright
Copyright © Cambridge University Press 2011

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

REFERENCES

Adamo, S. A. (2004). Estimating disease resistance in insects: phenoloxidase and lysozyme-like activity and disease resistance in the cricket Gryllus texensis. Journal of Insect Physiology 50, 209–216.CrossRefGoogle ScholarPubMed
Adamo, S. A., Jensen, M. and Younger, M. (2001). Changes in lifetime immunocompetence in male and female Gryllus texensis (formely G. integer): trade-offs between immunity and reproduction. Animal Behaviour 62, 417–425.CrossRefGoogle Scholar
Armitage, S. A. O., Thompson, J. J. W., Rolff, J. and Siva-Jothy, M. T. (2003). Examining costs of induced and constitutive immune investment in Tenebrio molitor. Journal of Evolutionary Biology 16, 1038–1044.CrossRefGoogle ScholarPubMed
Calleri, I. I. D., McGrail, V., Reid, E., Rosengaus, R. B., Vargo, E. L. and Traniello, J. F. A. (2006). Inbreeding and disease resistance in a social insect: effect of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis. Proceedings of the Royal Society of London, B 273, 2633–2640.Google Scholar
Contreras-Garduño, J., Córdoba-Aguilar, A., Lanz-Mendoza, H. and Cordero Rivera, A. (2009). Territorial behaviour and immunity are mediated by juvenile hormone: the physiological basis of honest signaling? Functional Ecology 23, 157–163.CrossRefGoogle Scholar
Contreras-Garduño, J., Lanz-Mendoza, H., Córdoba-Aguilar, A. (2007). The expression of a sexually selected trait correlates with different immune defense components and survival in males of the American rubyspot. Journal of Insect Physiology 53, 612–621.CrossRefGoogle ScholarPubMed
Córdoba-Aguilar, A., Contreras-Garduño, J., Peralta-Vázquez, H., Luna- González, A., Campa-Córdova, A. I. and Ascencio, F. (2006). Sexual comparisons in immune ability, parasite intensity and survival in two damselfly species. Journal of Insect Physiology 52, 861–869.CrossRefGoogle ScholarPubMed
Cotter, S. C., Kruuk, L. E. B. and Wilson, K. (2004). Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology 17, 421–429.CrossRefGoogle Scholar
Cotter, S. C. and Wilson, K. (2002). Heritability of immunocompetence in the caterpillar Spodoptera littoralis. Heredity 88, 229–234.CrossRefGoogle Scholar
Dromph, K. M. (2003). Collembolans as vectors of entomopathogenic fungi. Pedobiologia 47, 245–256.CrossRefGoogle Scholar
Fedorka, K. M., Zuk, M. and Mousseau, T. A. (2004). Immune suppression and the cost of reproduction in the ground cricket, Allonemobious socius. Evolution 56, 2478–2485.Google Scholar
Fisher, R. C. (1963). Oxygen requirements and the physiological suppression of supernumary insect parasitoids. Journal of Experimental Biology 38, 605–658.CrossRefGoogle Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Gerloff, C. U., Ottmer, B. K. and Schmid-Hempel, P. (2003). Effects of inbreeding on immune response and body size in a social insect, Bombus terrestris. Functional Ecology 17, 582–589.CrossRefGoogle Scholar
Gershman, S. N. (2008). Sex-specific differences in immunological costs of multiple mating in Gryllus vocalis field crickets. Behavioural Ecology 19, 810–815.CrossRefGoogle Scholar
Gillespie, J. P., Kanost, M. R. and Trenczek, T. (1997). Biological mediators of insect immunity. Annual Review of Entomology 42, 611–643.CrossRefGoogle ScholarPubMed
Gillespie, J. P. and Khachatourians, G. G. (1992). Characterization of Melanopplus sanguinipes after infection with Beauverina bassiana or wounding. Comparative Biochemistry and Physiology 103B, 455–463.Google Scholar
Gorman, M. J., Cornel, A. J., Collins, F. H. and Paskewitz, S. M. (1996). A shared genetic mechanism for melanotic encapsulation of CM-sephadex beads and the malaria parasite, Plasmodium cynomolgi B, in the mosquito Anopheles gambiae. Experimental Parasitology 84, 380–386.CrossRefGoogle ScholarPubMed
Gray, D. A. (1998). Sex differences in susceptibility of house crickets, Acheta domesticus, to experimental infection with Serratia liquefaciens. Journal of Invertebrate Pathology 71, 288–289.CrossRefGoogle ScholarPubMed
Gupta, A. P. (2001). Immunology of invertebrates: cellular. In Encyclopedia of Life Sciences. Nature Publishing Group, London, UK (www.els.net).Google Scholar
Kapari, L., Haukioja, E., Rantala, M. J. and Ruuhola, T. (2006). Immune defence of a defoliating insect interacts with induced plant defence during a population outbreak. Ecology 87, 291–296.CrossRefGoogle ScholarPubMed
Keller, L. F. and Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology & Evolution 17, 230–241.CrossRefGoogle Scholar
Kelly, C. D. and Jennions, M. D. (2009). Sexually dimorphic immune response in the harem polygynous Wellington tree weta Hemideina crassidens. Physiological Entomology 34, 174–179.CrossRefGoogle Scholar
Kivleniece, I., Krams, I., Krama, T., Daukste, J. and Rantala, M. J. (2010). Terminal investment in sexual signaling in male meal worm beetles. Animal Behaviour 80, 1015–1021.CrossRefGoogle Scholar
Köning, C. and Schmid-Hempel, P. (1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris. Proceedings of the Royal Society of London, B 260, 225–227.Google Scholar
Koskimäki, J., Rantala, M. J., Suhonen, J., Taskinen, J. and Tynkkynen, K. (2004). Immunocompetence and resource holding potential and immunocompetence in the damselfly Calopteryx virgo L. Behavioural Ecology 15, 169–173.CrossRefGoogle Scholar
Kruuk, L. E. B. (2004). Estimating genetic parameters in natural populations using the ‘animal model’. Philosophical Transactions of the Royal Society, B 359, 873–890.CrossRefGoogle ScholarPubMed
Kurtz, J., Wiesner, A., Götz, P. and Sauer, K. (2000). Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (insecta: mecoptera). Developmental and Comparative Immunology 24, 1–12.CrossRefGoogle ScholarPubMed
Lindsey, E. and Altizer, S. (2009). Sex differences in immune defenses and response to parasitism in monarch butterflies. Evolutionary Ecology 23, 607–620.CrossRefGoogle Scholar
Mallon, E. B., Loosli, R. and Schmid-Hempel, P. (2003). Specific versus nonspecific immune defense in the bumblebee, Bombus terrestris L. Evolution 57, 1444–1447.Google ScholarPubMed
Mietkiewski, R. and Tkaczuk, C. (1998). The spectrum and frequency of entomopathogenic fungi in litter, forest soil and arable soil. IOBC wprs Bulletin 21, 41–44.Google Scholar
Møller, A. P., Sorci, G. and Erritzøe, J. (1998). Sexual dimorphism in immune defense. American Naturalist 152, 605–619.CrossRefGoogle ScholarPubMed
Moret, Y. and Schmid-Hempel, P. (2000). Survival for immunity: the price of immune system activation for bumblebee workers. Science 290, 1166–1168.CrossRefGoogle Scholar
Moret, Y. and Siva-Jothy, M. T. (2003). Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society of London, B 270, 2475–2480.CrossRefGoogle ScholarPubMed
Mucklow, P. T., Vizoso, D. B., Jensen, K. H., Refardt, D. and Ebert, D. (2004). Variation for phenoloxidase activity and its relation to parasite resistance within and between populations of Daphnia magna. Proceedings of the Royal Society of London, B 271, 1175–1183.CrossRefGoogle ScholarPubMed
van Ooik, T., Rantala, M. J. and Saloniemi, I. (2007). Diet-mediated effects of heavy metal pollution on growth and immune response in the geometrid moth, Epirrita autumnata. Environmental Pollution 145, 348–354.CrossRefGoogle ScholarPubMed
Paskewitz, S. and Riehle, M. A. (1994). Response of Plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated sephadex beads. Developmental and Comparative Immunology 18, 369–375.CrossRefGoogle ScholarPubMed
Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A. and Suhonen, J. (2002). Do pheromones reveal immunocompetence? Proceedings of the Royal Society of London, B 269, 1681–1685.CrossRefGoogle ScholarPubMed
Rantala, M. J., Kortet, R., Kotiaho, J. S., Vainikka, A. and Suhonen, J. (2003 a). Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Functional Ecology 17, 534–540.CrossRefGoogle Scholar
Rantala, M. J., Kortet, R. and Vainikka, A. (2003 b). The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immunocompetence handicap principle. Proceedings of the Royal Society of London, B 270, 2257–2261.CrossRefGoogle ScholarPubMed
Rantala, M. J., Koskimäki, J., Taskinen, J., Tynkkynen, K. and Suhonen, J. (2000). Immunocompetence, developmental stability and wing spot size in the damselfly Calopteryx splendens L. Proceedings of the Royal Society of London, B 267, 2453–2457.CrossRefGoogle Scholar
Rantala, M. J. and Roff, D. A. (2005). An analysis of trade-off in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Functional Ecology 19, 323–330.CrossRefGoogle Scholar
Rantala, M. J. and Roff, D. A. (2006). Analysis of the importance of genotypic variation, metabolic rate, morphology, sex and development time on immune function in the cricket, Gryllus firmus. Journal of Evolutionary Biology 19, 834–843.CrossRefGoogle ScholarPubMed
Rantala, M. J. and Roff, D. A. (2007). Inbreeding and extreme outbreeding causes sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98, 329–336.CrossRefGoogle ScholarPubMed
Rantala, M. J., Roff, D. A. and Rantala, L. M. (2007). Forceps size and immune function in the european earwig Forficula auricularia. Biological Journal of Linnean Society 90, 509–516.CrossRefGoogle Scholar
Rolff, J. (2002). Bateman's principle and immunity. Proceedings of the Royal Society of London, B 269, 867–872.CrossRefGoogle ScholarPubMed
Rolff, J. and Siva-Jothy, M. T. (2002). Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences, USA 99, 9916–9918.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P. (2003). Variation in immune defence as a question of evolutionary ecology. Proceedings of the Royal Society of London, B 270, 357–366.CrossRefGoogle ScholarPubMed
Schwartz, A. and Koella, J. C. (2002). Melanization of Plasmodium falciparum and c-25 sephadex beads by field-caught Anopheles gambiae (Diptera : Culicidae) from southern Tanzania. Journal of Medical Entomology 39, 84–88.CrossRefGoogle ScholarPubMed
Schwarzenbach, G. A., Hosken, D. J. and Ward, P. I. (2005). Sex and immunity in the yellow dung fly Scathophaga stercoraria. Journal of Evolutionary Biology 18, 455–463.CrossRefGoogle ScholarPubMed
Schwarzenbach, G. A. and Ward, P. I. (2007). Phenoloxidase activity and pathogen resistance in yellow dung flies Scathophaga stercoraria. Journal of Evolutionary Biology 20, 2192–2199.CrossRefGoogle ScholarPubMed
Sheridan, L. A. D., Poulin, R., Ward, D. F. and Zuk, M. (2000). Sex differences in parasitic infections among arthropod hosts: is there a male bias? Oikos 88, 327–334.CrossRefGoogle Scholar
da Silva, C., Dunphy, G. B. and Rau, M. E. (2000). Interaction of hemocytes and prophenoloxidase system of fifth instar nymphs of Acheta domesticus with bacteria. Developmental and Comparative Immunology 24, 367–379.CrossRefGoogle ScholarPubMed
Siva-Jothy, M. T. and Thompson, J. W. (2002). Short-term nutrient deprivation affects adult immune function in the mealworm beetle, Tenebrio molitor L. Physiological Entomology 27, 206–212.CrossRefGoogle Scholar
Spielman, D., Brook, B. W., Briscoe, D. A. and Frankham, R. (2004). Does inbreeding and loss of genetic diversity decrease disease resistance? Conservation Genetics 5, 439–448.CrossRefGoogle Scholar
Stevens, L., Yan, G. and Pray, L. A. (1997). Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution 51, 2032–2039.CrossRefGoogle ScholarPubMed
Suhonen, J., Honkavaara, J. and Rantala, M. J. (2010). Activation of the immune system promotes insect dispersal in the wild. Oecologia 162, 541–547.CrossRefGoogle ScholarPubMed
Vainikka, A., Rantala, M. J., Seppälä, O. and Suhonen, J. (2007). Do male mealworm beetles, Tenebrio molitor, sustain the honesty of pheromone signals under immune challenge? Acta Ethologica 10, 63–72.CrossRefGoogle Scholar
Vainio, L., Hakkarainen, H., Rantala, M. J. and Sorvari, J. (2004). Individual variation in immune function in Formica exsecta: effect of nest, body size and sex. Evolutionary Ecology 18, 75–84.CrossRefGoogle Scholar
Valtonen, T. M., Viitaniemi, H. and Rantala, M. J. (2010). Copulation enhances resistance against an entomopathogenic fungi in the mealworm beetle Tenebrio molitor. Parasitology 137, 985–989.CrossRefGoogle ScholarPubMed
Washburn, J. O., Kirkpatrick, B. A. and Vokman, L. E. (1996). Insect protection against viruses. Nature, London 383, 767.CrossRefGoogle Scholar
Wilson, K., Cotter, S. C., Reeson, A. F. and Pell, J. K. (2001). Melanism and disease resistance in insects. Ecology Letters 4, 637–649.CrossRefGoogle Scholar
Yang, S., Ruuhola, T. and Rantala, M. J. (2007). Impacts of starvation on immune defense and other life history traits of an outbreaking geometrid, Epirrita autumnata: a possible ultimate trigger of the crash phase of population cycle. Annales Zoologici Fennici 44, 89–96.Google Scholar
Yourth, C. P., Forbes, M. and Smith, P. (2001). On understanding variation in immune expression of the damselflies Lestes spp. Canadian Journal of Zoology 79, 815–821.CrossRefGoogle Scholar
Yourth, C. P., Forbes, M. and Smith, B. P. (2002 a). Immune expression in a damselfly is related to time of season, not to fluctuating asymmetry or host size. Ecological Entomology 27, 123–128.CrossRefGoogle Scholar
Yourth, C. P., Forbes, M. and Smith, B. P. (2002 b). Sex differences in melanotic encapsulation responses (immunocompetence) in the damselfly Lestes forcipatus Rambur. Canadian Journal of Zoology 80, 1578–1583.CrossRefGoogle Scholar
Zuk, M. (1990). Reproductive strategies and disease susceptibility: an evolutionary viewpoint. Parasitology Today 6, 231–233.CrossRefGoogle ScholarPubMed
Zuk, M. and McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 1009–1024.CrossRefGoogle ScholarPubMed
Zuk, M., Simmons, L. W., Rotenberry, J. T. and Stoehr, A. M. (2004). Sex differences in immunity in two species of field crickets. Canadian Journal of Zoology 82, 627–634.CrossRefGoogle Scholar
Zuk, M. and Stoehr, A. M. (2002). Immune defence and host life history. American Naturalist 160, S9–S22.CrossRefGoogle ScholarPubMed