Evolution of Virulence: Malaria, a Case Study Prof. Andrew F. Read

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1 - - Evolution of Virulence: Evolution of Virulence: Andrew F. Read The University of Edinburgh Institutes of Evolutionary Biology & Immunology and Infection Research 1 Lecture outline Natural selection on malaria virulence Why are malaria parasites so virulent? Why aren t malaria parasites more virulent? Why bother? Possible selective effects of public health interventions Other diseases - and a plea 2 Malaria parasites on mosquito midgut Parasite dose Parasite genetics Death or survival Socio-economics Host genetics Acquired immunity 3 The screen versions of these slides have full details of copyright and acknowledgements 1

2 Malaria parasites in mammalian red blood cells 4 What selective factors act on parasite virulence? 5 Pathogen fitness function Parasite fitness Optimum Virulence 6 The screen versions of these slides have full details of copyright and acknowledgements 2

3 Growth rate (replacement rate/ parasite/cycle) In vitro growth rates of P. falciparum from Thai patients Uncomplicated malaria Chotivanich et al., 2000 Am. J. Trop. Med. Hyg. Severe malaria 7 What selective factors act on parasite virulence? What selective factors favour parasite virulence? 8 C57 mouse Parasites on a mosquito midgut A rodent malaria model: Plasmodium chabaudi 9 The screen versions of these slides have full details of copyright and acknowledgements 3

4 Genetic variation in virulence in P. chabaudi 4 Minimum 3 red cell density 2 (x 10 9 /ml) 1 0 CW AQ AD AJ AT BC ER 21 Minimum weight (g) CW AQ AD AJ AT BC ER Clone Mackinnon & Read Evolution 1999 Clone 10 Transmission experiments 11 Virulent strains transmit better 60 Clone mean Individual mouse Mosquitoes infected (%) Avirulent Weight loss (g) Virulent Mackinnon & Read Evolution The screen versions of these slides have full details of copyright and acknowledgements 4

5 Genetically diverse malaria infections are the norm.. B A. do virulent strains have a competitive advantage in hosts? 13 Testing outcome of in-host competition AJ 14 Virulent strains out compete less virulent strains Parasite density (avir) + AJ (mod) + AJ (vir) + AJ AJ Day post-infection This is true for across a range of clones - And it is relative virulence that matters De Roode, Pansini, Bell, Wargo, Hubie, Cheesman, Walliker & Read (2005); Bell, de Roode, Sim & Read (2006) 15 The screen versions of these slides have full details of copyright and acknowledgements 5

6 What selective factors act on parasite virulence? Enhanced infectiousness Within-host competition Affected by host immunity? 16 Experimental Serial passage evolution in immunised in naïve and mice immune increases hosts the speed of virulence evolution Naïve hosts Immunised hosts Anaemia lines Evolved Ancestor Evolved in non-immunes in immunes 5 lines Then measure the virulence of all ten evolved lines + ancestral lines What selective factors act on parasite virulence? Enhanced infectiousness Within-host selection Affected by host immunity? - Unaffected - Enhanced 18 The screen versions of these slides have full details of copyright and acknowledgements 6

7 What is maintaining the virulent Thai parasites? They compete better within hosts - They transmit better to new hosts Growth rate (replacement rate/ parasite/cycle) Uncomplicated malaria Chotivanich et al., 2000 Am. J. Trop. Med. Hyg. Severe malaria 19 What selective factors act on parasite virulence? Enhanced infectiousness Within-host selection affected by host immunity? - Unaffected - Enhanced 20 What factors select against virulent phenotypes? Host death 21 The screen versions of these slides have full details of copyright and acknowledgements 7

8 Parasite density (ml -1 x 10 6 ) Gametocyte density (ml -1 x 10 3 ) Death Parasite densities Day post-infection 80 Transmission 60 stages Day post-infection Mature gametocyte in peripheral blood 22 Individual patient.. Death (?) Parasite density (no. mm -3) Parasite density (no. mm -3) P. falciparum 100 Transmission stages All parasites Death (?) 100 Transmission stages Day post-infection P. vivax All parasites 23 What factors select against virulent phenotypes? Host death Vectors 24 The screen versions of these slides have full details of copyright and acknowledgements 8

9 Do more virulent clones kill more mosquitoes? Ferguson, Mackinnon, Chan & Read 2003 No! 25 What factors select against virulent phenotypes? Host death Vector death Host genetic diversity Growth vs. reproduction trade-offs Limited by host 26 What selective factors act on parasite virulence? Enhanced infectiousness Within-host competition?? 27 The screen versions of these slides have full details of copyright and acknowledgements 9

10 Why bother? Explain variation in disease pathogenicity in nature Predict direction of virulence evolution when diseases cross to new hosts Could some public health programs relax selection against virulence? 28 How does vaccination change selection on parasite virulence? Enhanced infectiousness Within-host competition Host death 29 Could vaccines weaken selection against virulent pathogens? + = + = Vaccines protect virulent pathogens from themselves Gandon, Mackinnon, Nee & Read 2001, 2003, The screen versions of these slides have full details of copyright and acknowledgements 10

11 Vaccination can promote the evolution of virulence by Protecting hosts and hence virulent strains Increasing in-host competitive advantage of virulence Leaky anti-disease vaccines may be evolutionary disasters waiting to happen Should aim to stop evolution: block infection or transmission 31 Does virulence evolution occur in response to vaccination? 32 Myxoma virus virulence in Australia Case-fatality rate (%) Virus virulence Rabbit resistance Data from Fenner & Fantini The screen versions of these slides have full details of copyright and acknowledgements 11

12 Human diseases? 34 Diphtheria - US Diphtheria incidence, mortality rates, and case-fatality ratio in the United States, 1920 to 1996 From Mortimer and Wharton in Plotkin and Orenstein 3 rd ed (1999) 35 Diphtheria - India W idespread vaccination Number of cases Case fatality rates (%) Clinical diphtheria in Infectious Diseases Hospital, Delhi, From Singh et al., Epidemiol. Infect. (1999) 36 The screen versions of these slides have full details of copyright and acknowledgements 12

13 Detecting any virulence evolution in human diseases will be a serious challenge Case fatality rates change (or don t change) for many reasons Problem of common garden Need proper molecular epidemiology of virulence determinants 37 For further reading, see: The University of Edinburgh Institutes of Evolutionary Biology & Immunology and Infection Research Mackinnon, M.J. & Read, A.F. 2004; Virulence in malaria: an evoluti onar y viewpoint; Philosophical Transacti ons of the Royal Society of London Biological Sciences; 359: Read, A.F., Gandon, S., Nee, S., & Mackinnon, M.J. 2004; The evoluti on of pathogen virulence in response to animal and public health interventions; In: Dronamraj, K. (ed.) Infectious Disease and Host-Pathogen Evolution; pp ; Cambridge University Press All references mentioned in this lecture, and updates, are availabl e on olog y.ac.uk/ or in the references cited there-in The screen versions of these slides have full details of copyright and acknowledgements 13

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