Trans-generational priming of resistance in wild flour beetles reflects the primed phenotypes of laboratory populations and is inhibited by co-infection with a common parasite

Functional Ecology

Volumn 29, Issue 8, 2015, Pages 1059-1069

  Tate, Ann T ^a,b   Graham, Andrea L ^a  

^a PRINCETON UNIVERSITY   (United States)

^b University of Houston   (United States)

Author keywords

Tribolium; Bacillus thuringiensis; Development; Gregarines; Life history trade offs

Indexed keywords

BEETLE; BIOLOGICAL DEVELOPMENT; DISEASE INCIDENCE; HOST-PATHOGEN INTERACTION; IMMUNE RESPONSE; INFECTIVITY; LIFE HISTORY TRAIT; PHENOTYPIC PLASTICITY; SURVIVORSHIP; WILD POPULATION;

ARTHROPODA; BACILLUS THURINGIENSIS; BACTERIA (MICROORGANISMS); COLEOPTERA; GREGARINIA; PROTOZOA; TRIBOLIUM (BEETLE);

EID: 84938415984     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12411     Document Type: Article

References (46)

1. Ayres, J.S. & Schneider, D.S. (2008) A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biology, 6, e305.
2. Bates, D., Maechler, M. & Dai, B. (2008) The lme4 package. Computer software manual. http://cran.r-project.org/web/packages/lme4/lme4.pdf.
3. Cisarovsky, G., Koch, H. & Schmid-Hempel, P. (2012) A field study on the influence of food and immune priming on a bumblebee-gut parasite system. Oecologia, 170, 1-8.
4. Clopton, R.E. (2009) Phylogenetic relationships, evolution, and systematic revision of the septate gregarines (Apicomplexa: Eugregarinorida: Septatorina). Comparative Parasitology, 76, 167-190.
5. Detwiler, J. & Janovy, J. Jr (2008) The role of phylogeny and ecology in experimental host specificity: insights from a eugregarine-host system. Journal of Parasitology, 94, 7-12.
6. Freitak, D., Heckel, D.G. & Vogel, H. (2009) Dietary-dependent trans-generational immune priming in an insect herbivore. Proceedings of the Royal Society B: Biological Sciences, 276, 2617-2624.
7. 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.
8. Gorman, M.J., Kankanala, P. & Kanost, M.R. (2004) Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Molecular Biology, 13, 19-24.
9. Haine, E.R., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008a) Antimicrobial defense and persistent infection in insects. Science, 322, 1257-1259.
10. Haine, E.R., Pollitt, L.C., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008b) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology, 54, 1090-1097.
11. Hernández López, J., Schuehly, W., Crailsheim, K. & Riessberger-Gallé, U. (2014) Trans-generational immune priming in honeybees. Proceedings of the Royal Society B: Biological Sciences, 281, 20140454.
12. Janovy, J. Jr, Detwiler, J., Schwank, S., Bolek, M.G., Knipes, A.K. & Langford, G.J. (2007) New and emended descriptions of gregarines from flour beetles (Tribolium spp. and Palorus subdepressus: Coleoptera, Tenebrionidae). Journal of Parasitology, 93, 1155-1170.
13. Kingsolver, J.G., Diamond, S.E., Seiter, S.A. & Higgins, J.K. (2012) Direct and indirect phenotypic selection on developmental trajectories in Manduca sexta. Functional Ecology, 26, 598-607.
14. Kurtz, J. & Franz, K. (2003) Innate defence: evidence for memory in invertebrate immunity. Nature, 425, 37-38.
15. Lazzaro, B.P., Sceurman, B.K. & Clark, A.G. (2004) Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science, 303, 1873-1876.
16. 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.
17. Locklin, J.L. & Vodopich, D.S. (2010) Patterns of gregarine parasitism in dragonflies: host, habitat, and seasonality. Parasitology Research, 107, 75-87.
18. McKean, K.A. & Lazzaro, B. (2011) The Costs of Immunity and the Evolution of Immunological Defense Mechanisms. Oxford University Press, Oxford.
19. Moreau, J., Martinaud, G., Troussard, J.-P., Zanchi, C. & Moret, Y. (2012) Trans-generational immune priming is constrained by the maternal immune response in an insect. Oikos, 121, 1828-1832.
20. Pedersen, A.B. & Babayan, S.A. (2011) Wild immunology. Molecular Ecology, 20, 872-880.
21. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. R foundation for statistical computing, Vienna, Austria.
22. Raymond, B.E.N., Sayyed, A.H., Hails, R.S. & Wright, D.J. (2007) Exploiting pathogens and their impact on fitness costs to manage the evolution of resistance to Bacillus thuringiensis. Journal of Applied Ecology, 44, 768-780.
23. Raymond, B., Johnston, P.R., Nielsen-LeRoux, C., Lereclus, D. & Crickmore, N. (2010) Bacillus thuringiensis: an impotent pathogen? Trends in Microbiology, 18, 189-194.
24. Reber, A. & Chapuisat, M. (2012) No evidence for immune priming in ants exposed to a fungal pathogen. PLoS ONE, 7, e35372.
25. Rodrigues, J., Brayner, F.A., Alves, L.C., Dixit, R. & Barillas-Mury, C. (2010) Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science, 329, 1353-1355.
26. Roth, O. & Kurtz, J. (2008) The stimulation of immune defence accelerates development in the red flour beetle (Tribolium castaneum). Journal of Evolutionary Biology, 21, 1703-1710.
27. 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 B: Biological Sciences, 276, 145-151.
28. Roth, O., Joop, G., Eggert, H., Hilbert, J., Daniel, J., Schmid-Hempel, P. et al. (2010) Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum. Journal of Animal Ecology, 79, 403-413.
29. Sadd, B.M. & Schmid-Hempel, P. (2006) Insect immunity shows specificity in protection upon secondary pathogen exposure. Current Biology, 16, 1206-1210.
30. Sadd, B.M. & Schmid-Hempel, P. (2007) Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Current Biology, 17, R1046-R1047.
31. Sadd, B.M. & Schmid-Hempel, P. (2009) A distinct infection cost associated with trans-generational priming of antibacterial immunity in bumble-bees. Biology Letters, 5, 798-801.
32. Sadd, B.M., Kleinlogel, Y., Schmid-Hempel, R. & Schmid-Hempel, P. (2005) Trans-generational immune priming in a social insect. Biology Letters, 1, 386-388.
33. Sorrentino, R.P., Carton, Y. & Govind, S. (2002) Cellular immune response to parasite infection in the Drosophila Lymph Gland is developmentally regulated. Developmental Biology, 243, 65-80.
34. Stearns, S.C. (1989) Trade-offs in life-history evolution. Functional Ecology, 3, 259-268.
35. Stubben, C. & Milligan, B. (2007) Estimating and analyzing demographic models using the popbio package in R. Journal of Statistical Software, 22, 1-23.
36. Tate, A.T. & Graham, A.L. (2014) Data from: Trans-generational priming of resistance in wild flour beetles reflects the primed phenotypes of laboratory populations and is inhibited by co-infection with a common parasite. Dryad Digital Repository, http://dx.doi.org/10.5061/dryad.8s3k6
37. Tate, A.T. & Rudolf, V.H.W. (2012) Impact of life stage specific immune priming on invertebrate disease dynamics. Oikos, 121, 1083-1092.
38. Thomas, A.M. & Rudolf, V.H.W. (2010) Challenges of metamorphosis in invertebrate hosts: maintaining parasite resistance across life-history stages. Ecological Entomology, 35, 200-205.
39. Tidbury, H.J., Best, A. & Boots, M. (2012) The epidemiological consequences of immune priming. Proceedings of the Royal Society B: Biological Sciences, 279, 4505-4512.
40. Tidbury, H.J., Pedersen, A.B. & Boots, M. (2010) Within and transgenerational immune priming in an insect to a DNA virus. Proceedings of the Royal Society B: Biological Sciences, 278, 871-876.
41. Trauer, U. & Hilker, M. (2013) Parental legacy in insects: variation of transgenerational immune priming during offspring development. PLoS ONE, 8, e63392.
42. Vorburger, C., Gegenschatz, S.E., Ranieri, G. & Rodriguez, P. (2008) Limited scope for maternal effects in aphid defence against parasitoids. Ecological Entomology, 33, 189-196.
43. Zanchi, C., Troussard, J.-P., 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.
44. Zanchi, C., Troussard, J.-P., Moreau, J. & Moret, Y. (2012) Relationship between maternal transfer of immunity and mother fecundity in an insect. Proceedings of the Royal Society B: Biological Sciences, 279, 3223-3230.
45. Ziauddin, J. & Schneider, D.S. (2012) Where does innate immunity stop and adaptive immunity begin? Cell Host & Microbe, 12, 394-395.
46. Ziegler, R. & Van Antwerpen, R. (2006) Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology, 36, 264-272.