Pathogen dose infectivity curves as a method to analyze the distribution of host susceptibility: A quantitative assessment of maternal effects after food stress and pathogen exposure

American Naturalist

Volumn 175, Issue 1, 2010, Pages 106-115

  Ben Ami, Frida ^a   Ebert, Dieter ^a   Regoes, Roland R ^b  

^a UNIVERSITY OF BASEL   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

Daphnia magna; Disease susceptibility; Frailty models; Pasteuria ramosa; Transgenerational effects

Indexed keywords

BACTERIUM; CRUSTACEAN; ECOLOGICAL MODELING; EPIDEMIOLOGY; FOOD AVAILABILITY; HOST-PARASITE INTERACTION; HOST-PATHOGEN INTERACTION; INFECTIVITY; NUMERICAL MODEL; PARASITIC DISEASE; QUANTITATIVE ANALYSIS; SPORE;

BACTERIA (MICROORGANISMS); DAPHNIA; DAPHNIA MAGNA; PASTEURIA RAMOSA;

ANIMAL; ARTICLE; BACILLALES; DAPHNIA; DISEASE PREDISPOSITION; FEMALE; FERTILITY; HOST PARASITE INTERACTION; PARASITOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; THEORETICAL MODEL;

ANIMALS; BACILLALES; DAPHNIA; DISEASE SUSCEPTIBILITY; FEMALE; FERTILITY; HOST-PARASITE INTERACTIONS; MODELS, THEORETICAL; STRESS, PHYSIOLOGICAL;

EID: 77449118984     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/648672     Document Type: Article

References (42)

1. Aalen, O. O. 1988. Heterogeneity in survival analysis. Statistics in Medicine 7:1121-1137.
2. Becker, N., and I. Marschner. 1990. The effect of heterogeneity on the spread of disease. Pages 90-103 in J. P. Gabriel, C. Lefèvre, and P. Picard, eds. Stochastic processes in epidemic theory. 2nd ed. Lecture Notes in Biomathematics 86. Springer, Berlin.
3. Ben-Ami, F., R. R. Regoes, and D. Ebert. 2008. A quantitative test of the relationship between parasite dose and infection probability across different host-parasite combinations. Proceedings of the Royal Society B: Biological Sciences 275:853-859.
4. Bernardo, J. 1996. Maternal effects in animal ecology. American Zoologist 36:83-105. (Pubitemid 27004112)
5. Brites, D., S. McTaggart, K. Morris, J. Anderson, K. Thomas, I. Colson, T. Fabbro, T. J. Little, D. Ebert, and L. Du Pasquier. 2008. The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Molecular Biology and Evolution 25:1429-1439.
6. Decaestecker, E., C. Lefever, L. De Meester, and D. Ebert. 2004. Haunted by the past: evidence for resting stage banks of microparasites and epibionts of Daphnia. Limnology and Oceanography 49:1355-1364.
7. Deredec, A., and F. Courchamp. 2003. Extinction thresholds in hostparasite dynamics. Annales Zoologici Fennici 40:115-130.
8. de Souza, P. N., R. J. Fateman, J. Moses, and C. Yapp. 2004. The Maxima book. http://maxima.sourceforge.net/docs/maximabook/maximabook-19-Sept-2004.pdf.
9. Duffy, M. A., and L. Sivars-Becker. 2007. Rapid evolution and ecological host-parasite dynamics. Ecology Letters 10:44-53.
10. Dwyer, G., J. S. Elkinton, and J. P. Buonaccorsi. 1997. Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model. American Naturalist 150:685-707.
11. Ebert, D. 1993. The trade-off between offspring size and number in Daphnia magna: the influence of genetic, environmental and maternal effects. Archiv für Hydrobiologie 90:453-473.
12. -. 1994. Fractional resource allocation into few eggs: Daphnia as an example. Ecology 75:568-571.
13. -. 2005. Ecology, epidemiology, and evolution of parasitism in Daphnia. National Library of Medicine, National Center for Biotechnology Information, Bethesda, MD. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=Books.
14. Ebert, D., P. Rainey, T. M. Embley, and D. Scholz. 1996. Development, life cycle, ultrastructure and phylogenetic position of Pasteuria ramosa Metchnikoff 1888: rediscovery of an obligate endoparasite of Daphnia magna Straus. Philosophical Transactions of the Royal Society B: Biological Sciences 351:1689-1701.
15. Ebert, D., C. D. Zschokke-Rohringer, and H. J. Carius. 1998. Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proceedings of the Royal Society B: Biological Sciences 265:2127-2134.
16. Ebert, D., M. Lipsitch, and K. L. Mangin. 2000. The effect of parasites on host population density and extinction: experimental epidemiology with Daphnia and six microparasites. American Naturalist 156:459-477.
17. Ebert, D., H. J. Carius, T. J. Little, and E. Decaestecker. 2004. The evolution of virulence when parasites cause host castration and gigantism. American Naturalist 164(suppl.):S19-S32.
18. Galvani, A. P., and R. M. May. 2005. Epidemiology: dimensions of superspreading. Nature 438:293-295.
19. Glazier, D. S. 1992. Effects of food, genotype, and maternal size and age on offspring investment in Daphnia magna. Ecology 73:910-926.
20. Green, J. 1974. Parasites and epibionts of Cladocera. Transactions of the Zoological Society of London 32:417-515.
21. Guinnee, M. A., S. A. West, and T. J. Little. 2004. Testing small clutch size models with Daphnia. American Naturalist 163:880-887.
22. Halloran, M. E., I. M. Longini Jr., and C. J. Struchiner. 1996. Estimability and interpretation of vaccine efficacy using frailty mixing models. American Journal of Epidemiology 144:83-97.
23. Hassell, M. P., and R. M. Anderson. 1984. Host susceptibility as a component in host-parasitoid systems. Journal of Animal Ecology 53:611-621.
24. Hougaard, P. 1986. A class of multivariate failure time distributions. Biometrika 73:671-678.
25. Little, T. J., and A. R. Kraaijeveld. 2004. Ecological and evolutionary implications of immunological priming in invertebrates. Trends in Ecology & Evolution 19:58-60.
26. Little, T. J., B. O'Connor, N. Colegrave, K. Watt, and A. F. Read. 2003. Maternal transfer of strain-specific immunity in an invertebrate. Current Biology 13:489-492.
27. Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359.
28. Longini, I. M., Jr., and M. E. Halloran. 1996. A frailty mixture model for estimating vaccine efficacy. Applied Statistics 45:165-173.
29. Minchella, D. J. 1985. Host life-history variation in response to parasitism. Parasitology 90:205-216.
30. Mitchell, S. E., and A. F. Read. 2005. Poor maternal environment enhances offspring disease resistance in an invertebrate. Proceedings of the Royal Society B: Biological Sciences 272:2601-2607.
31. Moret, Y. 2006. "Trans-generational immune priming": specific enhancement of antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proceedings of the Royal Society B: Biological Sciences 273:1399-1405.
32. Mousseau, T. A., and C. W. Fox. 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13:403-407.
33. R Development Core Team. 2005. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
34. Regoes, R. R., D. Ebert, and S. Bonhoeffer. 2002. Dose-dependent infection rates of parasites produce the Allee effect in epidemiology. Proceedings of the Royal Society B: Biological Sciences 269:271279.
35. Regoes, R. R., J. W. Hottinger, L. Sygnarski, and D. Ebert. 2003. The infection rate of Daphnia magna by Pasteuria ramosa conforms with the mass-action principle. Epidemiology and Infection 131:957-966.
36. Roth, O., B. M. Sadd, P. Schmid-Hempel, and J. Kurtz. 2009. Strainspecific priming of resistance in the red flour beetle, Tribolium castaneum. Proceedings of the Royal Society B: Biological Sciences 276:145-151.
37. Sadd, B. M., and P. Schmid-Hempel. 2007. Facultative but persistent trans-generational immunity via the mother's eggs in bumblebees. Current Biology 17:R1046-R1047.
38. Sadd, B. M., Y. Kleinlogel, R. Schmid-Hempel, and P. Schmid-Hempel. 2005. Trans-generational immune priming in a social insect. Biology Letters 1:386-388.
39. Tessier, A. J., and N. L. Consolatti. 1991. Resource quantity and offspring quality in Daphnia. Ecology 72:468-478.
40. Vorburger, C., S. E. Gegenschatz, G. Ranieri, and P. Rodriguez. 2008. Limited scope for maternal effects in aphid defence against parasitoids. Ecological Entomology 33:189-196.
41. Woolhouse, M. E., C. Dye, J.-F. Etard, T. Smith, J. D. Charlwood, G. P. Garnett, P. Hagan, et al. 1997. Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proceedings of the National Academy of Sciences of the USA 94:338-342.
42. Yates, A., R. Antia, and R. R. Regoes. 2006. How do pathogen evolution and host heterogeneity interact in disease emergence? Proceedings of the Royal Society B: Biological Sciences 273:3075-3083.