Page 101 - Science
P. 101
RESEARCH | REPORT
(24). Disentangling differences in susceptibility advantages to higher virulence demonstrated 22. J. S. Adelman, L. Kirkpatrick, J. L. Grodio, D. M. Hawley, Am. Nat.
versus infectiousness is a difficult problem in any here are relevant for a range of host and path- 181,674–689 (2013).
system, and we do not attempt to do so here. ogen systems, including humans. Overall, our re- 23. C. E. L. Delmas et al., Evol. Appl. 9, 709–725 (2016).
24. A. T. Tate, Oikos 126, 350–360 (2017).
Our model attributed differences in infection sults show that the same immune systems that 25. M. G. M. Gomes, A. Margheri, G. F. Medley, C. Rebelo, J. Math.
rates to what we term “host susceptibility” (h evolved to protect hosts from infection can drive Biol. 51,414–430 (2005).
in equations S2), as infection occurred through the evolution of more-harmful pathogens in 26. W. M. Geisler, S. Y. Lensing, C. G. Press, E. W. Hook 3rd,
J. Infect. Dis. 207, 1850–1856 (2013).
inoculation with equal pathogen doses. It is nature. 27. S. Hall et al., Pediatrics 109, 1068–1073 (2002).
likely that lower pathogen loads in hosts with 28. X. Castellsagué et al., J. Infect. Dis. 210, 517–534 (2014).
prior exposure (Fig. 1B) will also lead to lower REFERENCES AND NOTES 29. R. Casais et al., Vet. Parasitol. 203, 173–183 (2014).
infectiousness and thus less transmission by 1. S. Gandon, M. J. Mackinnon, S. Nee, A. F. Read, Nature 414, 30. M. C. De Jong, W. H. van der Poel, J. A. Kramps, A. Brand,
J. T. van Oirschot, Am. J. Vet. Res. 57, 628–633 (1996).
those individuals. Although our models al- 751–756 (2001). 31. A. Sabó, D. Blaškovic, Acta Virol. 14,17–24 (1970).
lowed for higher transmission rates for more- 2. M. J. Mackinnon, S. Gandon, A. F. Read, Vaccine 26 (suppl. 3), 32. J. L. Schulman, E. D. Kilbourne, J. Bacteriol. 89,170–174 (1965).
virulent strains in both scenarios (Fig. 3), we C42–C52 (2008). 33. M. D. Moody, C. M. Downs, J. Bacteriol. 70, 297–304 (1955).
did not vary transmission rates with host prior 3. P. D. Williams, T. Day, Mol. Ecol. 17, 485–499 (2008). 34. M. P. Davenport, G. T. Belz, R. M. Ribeiro, Trends Immunol. 30,
4. V. C. Barclay et al., PLOS Biol. 10, e1001368 (2012).
61–66 (2009).
exposure. Further, although our data support 5. A. F. Read et al., PLOS Biol. 13, e1002198 (2015). 35. A. E. Fleming-Davies, V. Dukic, V. Andreasen, G. Dwyer, Ecol. Lett.
reduced infection length with prior exposure 6. C. R. Faustino et al., J. Anim. Ecol. 73, 651–669 (2004). 18,1252–1261 (2015).
(fig. S2), we were unable to robustly quantify 7. J. S. Adelman, C. Mayer, D. M. Hawley, J. Avian Biol. 48,
519–528 (2017).
this effect and thus assumed equal infection ACKNOWLEDGMENTS
8. A. A. Dhondt et al., EcoHealth 3, 95 (2006).
lengths. Thus, our model is likely conservative, 9. A. A. Dhondt, K. V. Dhondt, D. M. Hawley, C. S. Jennelle, This work is dedicated to the memory of Paul Williams, who
as selection for higher virulence should be even Avian Pathol. 36,205–208 (2007). inspired us all with his insights and dedication. We thank
10. D. M. Hawley et al., PLOS Biol. 11, e1001570 (2013). L. Kirkpatrick, J. Adelman, S. Moyers, and numerous undergraduates
stronger if infectiousness and infection length for technical assistance. D. J. Páez and three anonymous
11. A. A. Dhondt, K. V. Dhondt, W. M. Hochachka, D. H. Ley,
also vary with host prior exposure. reviewers provided helpful comments on the manuscript. This work
D. M. Hawley, Avian Dis. 61, 437–441 (2017).
Previous studies argue for great care in design- 12. A. E. Leon, D. M. Hawley, EcoHealth 14,793–804 (2017). was funded through NIH grant 5R01GM105245 to D.M.H. under
ing vaccines because incomplete protection can 13. K. V. Sydenstricker, A. A. Dhondt, D. H. Ley, G. V. Kollias, the NIH-NSF-USDA Ecology and Evolution of Infectious Diseases
program. Birds were captured under permits from the Virginia
select for increased virulence in the targeted path- J. Wildl. Dis. 41, 326–333 (2005). Department of Game and Inland Fisheries (044569) and the Downloaded from
ogens (1, 3, 5). Our study suggests that pathogens 14. M. G. Netea, J. Quintin, J. W. M. van der Meer, Cell Host U.S. Fish and Wildlife Service (MB158404-1). All data and code
Microbe 9, 355–361 (2011).
can readily evolve toward higher virulence due 15. P. D. Williams, A. P. Dobson, K. V. Dhondt, D. M. Hawley, to understand and assess the conclusions of this research are
simply to the imperfect nature of host immune A. A. Dhondt, J. Evol. Biol. 27, 1271–1278 (2014). included in the main text or are available via Dryad Digital
Repository (doi:10.5061/dryad.435h5).
memory, whether via adaptive or innate responses 16. P. M. Nolan, G. E. Hill, A. M. Stoehr, Proc. R. Soc. London Ser. B
(14). Despite historical focus on the small subset 265, 961–965 (1998). SUPPLEMENTARY MATERIALS
17. C. S. Jennelle, E. G. Cooch, M. J. Conroy, J. C. Senar, Ecol. Appl.
of pathogens that confer complete and lifelong 17, 154–167 (2007). www.sciencemag.org/content/359/6379/1030/suppl/DC1
immunity, incomplete immunity following infec- 18. W. M. Hochachka et al., Proc. R. Soc. London Ser. B 280, Materials and Methods
tion is widespread in humans (25–28)and other 20131068 (2013). Supplementary Text
Figs. S1 to S4
animals (29–32). Because therearelikelymany 19. F. Fenner, F. N. Ratcliffe, Myxomatosis (Cambridge Univ. Press, Tables S1 to S5 http://science.sciencemag.org/
Cambridge, 1965).
systems where more-virulent pathogen strains 20. C. Bonneaud et al., Proc. Natl. Acad. Sci. U.S.A. 108, References (36–49)
stimulate stronger immune responses and thus 7866–7871 (2011). 30 June 2017; accepted 12 January 2018
provide stronger protection (33, 34), the fitness 21. D. M. Hawley et al., J. Evol. Biol. 23, 1680–1688 (2010). 10.1126/science.aao2140
on March 1, 2018
Fleming-Davies et al., Science 359, 1030–1033 (2018) 2 March 2018 4of4

