Theoretical Ecology

, Volume 5, Issue 2, pp 211–217 | Cite as

Local transmission processes and disease-driven host extinctions

  • Alex Best
  • Steve Webb
  • Janis Antonovics
  • Mike Boots
Original paper


Classic infectious disease theory assumes that transmission depends on either the global density of the parasite (for directly transmitted diseases) or its global frequency (for sexually transmitted diseases). One important implication of this dichotomy is that parasite-driven host extinction is only predicted under frequency-dependent transmission. However, transmission is fundamentally a local process between individuals that is determined by their and/or their vector’s behaviour. We examine the implications of local transmission processes to the likelihood of disease-driven host extinction. Local density-dependent transmission can lead to parasite-driven extinction, but extinction is more likely under local frequency-dependent transmission and much more likely when there is active local searching behaviour. Density-dependent directly transmitted diseases spread locally can therefore lead to deterministic host extinction, but locally frequency-dependent passive vector-borne diseases are more likely to cause extinctions. However, it is active searching behaviour either by a vector or between sexual partners that is most likely to cause the host to go extinct. Our work emphasises that local processes are essential in determining parasite-driven extinctions, and the role of parasites in the extinction of rare species may have been underplayed due to the classic assumption of global density-dependent transmission.


Transmission Spatial structure Host–parasite Extinction 

Supplementary material

12080_2011_111_MOESM1_ESM.pdf (102 kb)
ESM 1 (PDF 101 kb)


  1. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280:361–367PubMedCrossRefGoogle Scholar
  2. Anderson RM (1981) Population dynamics of indirectly transmitted disease agents: the vector component. In: McKelvey JJ Jr, Eldridge BF, Maramorosch K (eds) Vectors of Disease Agents. Praeger, NY, pp 13–43Google Scholar
  3. Antonovics J (2009) The effect of sterilizing diseases on host abundance and distribution along environmental gradients. Proc R Soc Lond B Biol Sci 276:1443–1448CrossRefGoogle Scholar
  4. Antonovics J, Iwasa Y, Hassell MP (1995) A generalized model of parasitoid, venereal, and vector-based transmission processes. Am Nat 145:661–675CrossRefGoogle Scholar
  5. Baudoin M (1975) Host castration as a parasitic strategy. Evolution 29:335–352CrossRefGoogle Scholar
  6. Boots M, Begon M (1994) Resource limitation and the lethal and sub-lethal effects of a viral pathogen in the Indian meal moth, Plodia interpunctella. Ecol Entomol 19:319–326CrossRefGoogle Scholar
  7. Boots M, Sasaki A (1999) ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc R Soc Lond B Biol Sci 266:1933–1938CrossRefGoogle Scholar
  8. Boots M, Sasaki A (2000) The evolutionary dynamics of local infection and global reproduction in host-parasite interactions. Ecol Lett 3:181–185CrossRefGoogle Scholar
  9. Boots M, Sasaki A (2002) Parasite-driven extinction in spatially explicit host-parasite systems. Am Nat 159:706–713PubMedCrossRefGoogle Scholar
  10. Boots M (2004) Modelling insect diseases as functional predators. Physiol Entomol 29:237–239CrossRefGoogle Scholar
  11. Bremermann HJ, Pickering J (1983) A game-theoretical model of parasite virulence. J Theor Biol 100(3):411–426PubMedCrossRefGoogle Scholar
  12. Bremermann HJ, Thieme H (1989) A competitive exclusion principle for pathogen virulence. J Math Biol 27:179–190PubMedCrossRefGoogle Scholar
  13. Cavalli-Sforza LL (1958) Some data on the genetic structure of human populations. Proc 10th Int Cong Genet 1:389–407Google Scholar
  14. Clay K (1991) Parasitic castration of plants by fungi. Trends Ecol Evol 6:162–166PubMedCrossRefGoogle Scholar
  15. Dieckmann, U., Law, R. and Metz, J. A. J. (2000). The geometry of ecological interactions: simplifying spatial complexity. Cambridge University PressGoogle Scholar
  16. Doedel, E.J., Champneys, A.R., Fairgrieve, T.R., Kuznetsov,Y.A., Sandstede, B.,Wang, X.J. (1997). AUTO 97: Continuation and bifurcation software for ordinary differential equations. Available from Accessed 18 Jan 2010
  17. Getz WM, Pickering J (1983) Epidemic models: thresholds and population regulation. Am Nat 121(6):892–898CrossRefGoogle Scholar
  18. Hassell MP (1978) The dynamics of arthropod predator–prey systems. Princeton University Press, PrincetonGoogle Scholar
  19. Hassell, M. P. (2000). The Spatial and Temporal Dynamics of Host-Parasitoid Interactions. Oxford University Press.Google Scholar
  20. Jaenike J (1992) Mycophagous Drosophila and their nematode parasites. Am Nat 139:893–906CrossRefGoogle Scholar
  21. Keeling MJ (1999) The effects of local spatial structure on epidemiological invasions. Proc R Soc Lond B Biol Sci 266:859–867CrossRefGoogle Scholar
  22. Kermack WO, McKendrick AG (1927) Contributions to the mathematical theory of epidemics-1. Proc R Soc Lond B Biol Sci 115A:700–721Google Scholar
  23. Kuris AM (1974) Trophic interactions: similarity of parasitic castrators to parasitoids. Q Rev Biol 49:129–148CrossRefGoogle Scholar
  24. Lafferty KD, Kuris AM (1996) Biological control of marine pests. Ecology 77:1989–2000CrossRefGoogle Scholar
  25. Lafferty KD, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25:564–572PubMedCrossRefGoogle Scholar
  26. Levin S, Pimental D (1981) Selection of intermediate rates of increase in parasite-host systems. Am Nat 117(3):308–315CrossRefGoogle Scholar
  27. Lockhart AB, Thrall PH, Antonovics J (1996) The distribution and characteristics of sexually transmitted diseases in animals: ecological and evolutionary implications. Biol Rev Camb Philos Soc 71:415–471PubMedCrossRefGoogle Scholar
  28. Matsuda H, Ogita N, Sasaki A, Sato K (1992) Statistical mechanics of population: the lattice Lotka-Volterra model. Prog Theor Phys 88(6):1035–1044CrossRefGoogle Scholar
  29. May RM, Anderson RM (1979) Population biology of infectious diseases: part II. Nature 280:455–461PubMedCrossRefGoogle Scholar
  30. McCallum H, Dobson A (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends Ecol Evol 10:190–194PubMedCrossRefGoogle Scholar
  31. Meyers LA, Pourbohloul B, Newman MEJ, Skowronski DM, Brunham RC (2005) Network theory and SARS: predicting outbreak diversity. J Theor Biol 232:71–81PubMedCrossRefGoogle Scholar
  32. Ovaskainen O, Cornell SJ (2006) Space and stochasticity in population dynamics. PNAS 103:12781–12786PubMedCrossRefGoogle Scholar
  33. Pedersen AB, Jones KE, Nunn CL, Altizer S (2007) Infectious diseases and extinction risk in wild mammals. Conserv Biol 21:1269–1279PubMedCrossRefGoogle Scholar
  34. Rand DA, Keeling M, Wilson HB (1995) Invasion, stability and evolution to criticality in spatially extended, artificial host-pathogen ecologies. Proc R Soc Lond B Biol Sci 259:55–63CrossRefGoogle Scholar
  35. Roy M, Pascual M (2006) On representing network heterogeneities in the incidence rate of simple epidemic models. Ecol Complex 3:80–90CrossRefGoogle Scholar
  36. Rudolf VHW, Antonovics J (2005) Species coexistence and pathogens with frequency-dependent transmission. Am Nat 166:112–118PubMedCrossRefGoogle Scholar
  37. Ryder JJ, Miller MR, White A, Knell RJ, Boots M (2007) Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116:2017–2026CrossRefGoogle Scholar
  38. Sato K, Matsuda H, Sasaki A (1994) Pathogen invasion and host extinction in lattice structured populations. J Math Biol 32:251–268PubMedCrossRefGoogle Scholar
  39. Turner J, Begon M, Bowers RG (2003) Modelling pathogen transmission: the interrelationship between local and global approaches. Proc R Soc Lond B Biol Sci 270:105–112CrossRefGoogle Scholar
  40. Webb SD, Keeling MJ, Boots M (2007a) Host-parasite interactions between the local and the mean-field: how and when does spatial population structure matter? J Theor Biol 249:140–152PubMedCrossRefGoogle Scholar
  41. Webb SD, Keeling MJ, Boots M (2007b) Spatially extended host-parasite interactions: The role of recovery and immunity. Theor Popul Biol 71:251–266PubMedCrossRefGoogle Scholar
  42. Wennstrom A, Ericson L (2003) The concept of sexually transmitted diseases in plants: definition and applicability. Oikos 100:397–402CrossRefGoogle Scholar
  43. White A, Begon M, Bowers R (1999) The spread of infection in seasonal insect-pathogen systems. Oikos 85:487–498CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Alex Best
    • 1
  • Steve Webb
    • 2
  • Janis Antonovics
    • 3
  • Mike Boots
    • 1
  1. 1.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  2. 2.Department of Mathematics and StatisticsUniversity of StrathclydeGlasgowUK
  3. 3.Department of BiologyUniversity of VirginiaCharlottesvilleUSA

Personalised recommendations