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Multi-host, multi-parasite dynamics – Andy Dobson

Multi-host, multi-parasite dynamics – Andy Dobson. Many thanks to Peter Hudson Mercedes Pascual and Stefano Allesina Anieke van Leeuwen & Claire Standley Kevin Lafferty, Jennifer Dunne, and Giulio de Leo Many, many NCEAS working groups.

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Multi-host, multi-parasite dynamics – Andy Dobson

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  1. Multi-host, multi-parasite dynamics – Andy Dobson Many thanks to Peter Hudson Mercedes Pascual and Stefano Allesina Aniekevan Leeuwen & Claire Standley Kevin Lafferty, Jennifer Dunne, and Giulio de Leo Many, many NCEAS working groups  Ancient cures for diseases will reveal themselves once more. Mathematical discoveries glimpsed and lost to view will have their time again.” ― Tom Stoppard, Arcadia

  2. Tom Stoppard, Arcadia • “It's the best possible time to be alive, when almost everything you thought you knew is wrong.”  • “It's the wanting to know that makes us matter.”  • “We're better at predicting events at the edge of the galaxy or inside the nucleus of an atom than whether it'll rain on auntie's garden party three Sundays from now.” 

  3. Outline “The unpredictable and the predetermined unfold together to make everything the way it is.” ― Tom Stoppard, Arcadia • Parasite diversity and food webs • Parasites with multiple hosts • Parasites with sequential multiple hosts • Parasite communities : dynamics x immunity.

  4. Food webs and parasites.Carpinteria salt marsh, California Traditional resource-consumer web. Trophic levels = 3.77 Food web that incudes basic parasite links Trophic levels = 5.68 Dunne et al, PLoS Biology, (2013)

  5. Parasites are central to healthy ecosystems!! (Hudson et al, 2005) Number of trophic levels = 7.16 Includes parasite trophic links Free-living species – red : Macroparasites – blue Not yet added microparasites or “microbiome” Dunne et al, 2013, PLoS Biology.

  6. Parasites and food webs • Food webs are even more complex when we include parasites: • Many more species -> more links • Simple cascade model is instantly falsified • How does this effect May’s (1973) stability-complexity paradigm? • Main focus of this talk is to consider how work since “Ro or Not Newton” has developed insights into this central problem in Ecology.

  7. . Stability criteria for different types of interaction S Allesina & S Tang Nature000, 1-4 (2012) doi:10.1038/nature10832 Stability Diversity - Number of Species

  8. Multiple host species I. • What happens when multiple host species share the same pathogen ? • Rinderpest would be classic example here – eradicated since last Newton… • Also rabies and other species that jump between hosts. • Can be modeled with coupled sets of SI and SIR equations

  9. Walter Plowright Walter Plowright, CMG, FRS[1], FRCVS (born 20 July 1923, Holbeach, Lincolnshire – 19 February 2010 London[2]) was an English veterinary scientist who devoted his career to the eradication of the cattle plague rinderpest. Dr Plowright received the 1999 World Food Prize for his development of tissue culture rinderpest vaccine (TCRV), the key element in the quest to eliminate rinderpest.[3]Rinderpest became the first animal disease to be eliminated worldwide

  10. Multiple host species I. • What happens when multiple host species share the same pathogen ? • Rinderpest would be classic example here – eradicated since last Newton… • Also rabies and other species that jump between hosts. • Can be modeled with coupled sets of SI and SIR equations

  11. A cartoon of the talk…..

  12. Rinderpest – Serengeti

  13. Basic model structure.. Susceptibles Allometric scaling of all birth and death rates Within Between Infecteds Scale virulence as a proportion of life expectancy Between species transmission

  14. De Leo and Dobson (1996)

  15. Buffering: dynamics in DD case Susceptible density Between sps. transmission Time

  16. Buffering: dynamics in DD case Max./Min. susceptible density Between/within species transmission

  17. Multiple hosts species II • Obligatory and sequential use of multiple hosts to complete complex life cycle • Can next-generation methods be useful here? • Food-web perspective • Long loops ‘may’ be stabilizing • Often multiple alternative hosts on same trophic level • Types of pathogen where most likely to see dilution effects

  18. Cestodes of the Serengeti (host)

  19. Multiple definitive hosts

  20. Multiple intermediate hosts

  21. Cestodes of the Serengeti…. Beetles….

  22. Insight: There are multiple ways to go around the life cycle…

  23. Insight 2: Ro is a root of the sum of all possible routes around the life cycle…..hmmmm! But why does the magnitude of the root keep changing

  24. ..then a pattern began to emerge… Although these expressions look at first sight slightly incongruous, they both have the same properties in that they define R0 as the ‘n-th’ root of the sum of all the possible transmission routes around the life cycle; notice that ‘n’ is the number of trophic levels that the parasite passes through in the course of its life cycle. This creates a beautiful link to the need to study complex life cycles parasites within a food-web context.

  25. Ribeiroia ondatrae Flatworm Life Cycle Contact Elizabeth Morales ScienceArt.com

  26. Convert to a more theory friendly format….

  27. Multiple Parasite species • Communities of parasites that share the same hosts species • Initial work by Robert’s and Dobson at Newton • Much current interest in role that immunity plays • BUT, current work tends to ignore earlier work on aggregation and persistence. • So need to find a framework to bring the two together!

  28. Anderson and May macroparasite models – with multiple parasites • Original two parasite version developed by Dobson (1985), extended to n-species by Roberts and Dobson (1995) • Simple graphical ways for initially considering this with two species • Multi-parasite version has underlying structural similarities to Hubbell’s Neutral theory.

  29. Phase plane for simple competition Coexistence requires And vice versa for B2 and B1 Thus coexistence requires k’>>1 Both species have to be aggregated

  30. Interference competitioneg (nearly) all immunological interactions!! Here we assume competition is asymmetrical: B can exclude A, but not vice versa. Coexistence still requires A2>A1 and B2>B1

  31. Synergistic interactionsmost of the other immunological interactions Coexistence still requires A2>A1 and B2>B1 So we need to know how immunity impacts virulence and aggregation

  32. N-species of parasite Note – curiously related to “Neutral theory of Ecology - Hubbell……

  33. Both parasite species co-exist Intrinsic growth rate of parasite species 2 Intrinsic growth rate of parasite species 1.

  34. Parasite Community Dynamics2. Interference competition Direct competition Worm 1 What is the nature of competition? Competition for space Competition for food Competition via excreted material Food -ve Excreta -ve Stomach Space -ve When should we expect competition? Applying the findings from community ecology…this should be greater when parasites are related Interestingly this contrasts with exploitation competition Worm 3 Worm 2 Food -ve appears +ve Small Intestine Isabella Cattadori’s work on helminth Communities in rabbits with and w/o Myxomatosis – P. Hudson on Thursday Worm 4 Large Intestine

  35. Mixed macro and micro parasite models • Some initial work by Andy Fenton.

  36. Within Host dynamics of parasite communities will be driven by Immunological dynamics regulated by Th1-Th2 cytokine interactions • Joint work with my Post-Docs : • Anieke van Leeuwen • and earlier explorations with Claire Standley

  37. Background • Th1 cytokines -> microparasite infection control [viruses, bacteria, fungi, protozoa] • Th2 cytokines -> macroparsite infection control [helminths, nematodes] • Th1 and Th2 responses are supposed to have mutual inhibitory effects (competition) • Hosts are often co-infected with multiple parasite species (e.g. Fenton & Pedersen 2007) • How does the interaction of the th1 and th2 immune responses work out? • => Mathematical modeling

  38. Processes in detail + After Yates et al. 2000 - JTB IL-2 + + IL-2 IFN-γ Th1 + + IL-12 AICD IFN-γ + Th1 IL-2 APC - Th - TGF-β IFN-γ IFN-γ - + IL-10 - IL-4 Th2 IL-4 + IL-10 - Th2 - IL-2 TGF-β + IL-4 AICD +

  39. Tempting to think of this as a food-web

  40. Simplified representation + + Th1 + AICD Th1 APC Th - - + Th2 + - AICD Th2 + After Yates et al. 2000 - JTB

  41. Activation + + Th1 + AICD Th1 APC Th - - + Th2 + - Th1 AICD Th2 + Th2 Yates et al. 2000 - JTB

  42. Proliferation + + Th1 + AICD Th1 APC Th - - + Th2 + - AICD Th2 + Yates et al. 2000 - JTB

  43. Mortality + + Th1 + AICD Th1 APC Th - - + Th2 + - AICD Th2 + Yates et al. 2000 - JTB

  44. Model equations + + Th1 + AICD Th1 APC Th - - + Th2 + - AICD Th2 + Yates et al. 2000 - JTB

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