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Plant disease spread and
        establishment in small-size
             directed networks

                    Mathieu Moslonka-Lefebvre,
                    Marco Pautasso & Mike Jeger
                     Imperial College London,
                           Silwood Park

               IEW 10, Geneva, NY - 10 June 2009

Photo: Ottmar Holdenrieder
Outline of the talk
    1. The relevance of networks
       for disease epidemiology

2. Case study: Phytophthora ramorum

  3. Simulations of disease spread
   in small-size directed networks

          4. Conclusions
Disease spread in
                                                                  a globalized world




                             number of passengers per day
Hufnagel et al. (2004) Forecast and control of epidemics in a globalized world. PNAS
Understanding human mobility patterns




Matisoo-Smith et al. (1998) Patterns of prehistoric human mobility
in Polynesia indicated by mtDNA from the Pacific rat. PNAS
Understanding plant mobility patterns




Vendramin et al. (2008) Genetically depauperate but widespread:
the case of an emblematic Mediterranean pine. Evolution
Plant nurseries
as hubs




                                                               100 km
2000-2004
Brenn et al. (2008) Community structure of Phialocephala fortinii s. lat.
in European tree nurseries, and assessment of the potential of the
seedlings as dissemination vehicles. Mycological Research
Epidemiology is just one of the
                       many applications of network theory

Network pictures from:            NATURAL
Newman (2003)
SIAM Review                                     food webs

                                             cell
                                          metabolism
                                                  neural                    Food web of Little Rock
                                                 networks                     Lake, Wisconsin, US
                                                 ant nests      sexual
                                                             partnerships
                                               DISEASE
                                               SPREAD
                                                              family
                                     innovation              networks
Internet                                flows co-authorship                                  HIV
structure                     railway urban road nets                                      spread
                 electrical  networks networks                                            network
               power grids                                telephone calls
                                                WWW
          computing          airport Internet              E-mail
                                                                     committees
            grids           networks     software maps    patterns
TECHNOLOGICAL                                                                     SOCIAL
modified from: Jeger et al. (2007) New Phytologist
Outline of the talk
    1. The relevance of networks
       for disease epidemiology

2. Case study: Phytophthora ramorum

  3. Simulations of disease spread
   in small-size directed networks

          4. Conclusions
from: McKelvey et al. (2007) SOD Science Symposium III
P. ramorum
Map from www.suddenoakdeath.org    confirmations on
        Kelly, UC-Berkeley
                                  the US West Coast
                                    vs. national risk




                                        Hazard map:
                                       Koch & Smith,
                                      3rd SOD Science
                                     Symposium (2007)
Phytophthora ramorum in England & Wales (2003-2006)
                    511 nurseries/            168 historic gardens/
                    garden centres                 woodlands 122
                                    85
                                   2003-                      46
                                                              2003-
                                 Jun 2008                     Jun
                                    426                       2008




Climatic match courtesy of                   Outbreak maps courtesy of
Richard Baker, CSL, UK               David Slawson, PHSI, DEFRA, UK
Outline of the talk
    1. The relevance of networks
       for disease epidemiology

2. Case study: Phytophthora ramorum

  3. Simulations of disease spread
   in small-size directed networks

          4. Conclusions
Fraction of population infected (l) as a function of ρ0


                                                                              uniform degree
                                                                               distribution


                                                                            scale-free network
                                                                              with P(i) ≈ i-3


                                                                      ρ0 is coincident with R0
                                                                       for a uniform degree
                                                                             distribution;
                                                                     for a scale-free network,
                                                                          theory says that
                                                                       R0 = ρ0 + [1 + (CV)2],
                                                                          where CV is the
                                                                     coefficient of variation of
                                                                      the degree distribution
  May (2006) Network structure and the biology of populations. Trends in Ecology & Evolution
Simple model of infection spread (e.g. P. ramorum) in a network
                   pt probability of infection transmission
                   pp probability of infection persistence

          node 1       2       3      4       5     6        7   8   … 100

 step 1




 step 2




 step 3
  …

 step n
The four basic types of network structure used
 SIS Model, 100 Nodes, directed networks,
 P [i (x, t)] = Σ {p [s] * P [i (y, t-1)] + p [p] * P [i (x, t-1)]}




 local                                     small-
                                           world




random                                    scale-free
Examples of epidemic development in four kinds of
                                directed networks of small size (at threshold conditions)
sum probability of infection across all nodes


                                                1.2                                              40   1.2                          25


                                                                                     local       35                  small-world




                                                                                                                                        % nodes with probability of infection > 0.01
                                                1.0                                                   1.0
                                                                                                                                   20
                                                                                                 30

                                                0.8                                                   0.8
                                                                                                 25
                                                                                                                                   15

                                                0.6                                              20   0.6

                                                                                                                                   10
                                                                                                 15
                                                0.4                                                   0.4

                                                                                                 10
                                                                                                                                   5
                                                0.2                                                   0.2
                                                                                                 5


                                                0.0                                              0    0.0                          0
                                                      1   51        101        151         201              1   26   51     76
                                                                                                      1.2                          80
                                                1.6                                              60


                                                                                                                     scale-free    70

                                                                               random
                                                1.4
                                                                                                      1.0
                                                                                                 50

                                                1.2                                                                                60

                                                                                                 40   0.8
                                                1.0                                                                                50


                                                0.8                                              30   0.6                          40


                                                0.6                                                                                30
                                                                                                 20   0.4

                                                0.4                                                                                20

                                                                                                 10   0.2
                                                0.2                                                                                10


                                                0.0                                              0    0.0                          0
                                                      1        26         51          76                    1   26   51     76

                             from: Pautasso & Jeger (2008) Ecological Complexity
Lower epidemic threshold for scale-free networks
                      with positive correlation between in- and out-degree
                             1.00
                                                                        local
probability of persistence



                                                                        random
                             0.75                                       small-world
                                                                        scale-free (two-way)
                                                                        scale-free (uncorrelated)
                             0.50                                       scale-free (one way)



                             0.25



                             0.00
                                0.00              0.25           0.50            0.75               1.00
                                       Epidemic      probability of transmission
                                       does not
                                       develop                                     Epidemic develops
         modified from: Pautasso & Jeger (2008) Ecological Complexity
Lower epidemic threshold for two-way scale-free networks
        (unless networks are sparsely connected)
                                               N replicates = 100;
                                             error bars are St. Dev.;
                                             different letters show
                                              sign. different means
                                                    at p < 0.05




from: Moslonka-Lefebvre et al. (submitted)
1.0                                                              1.0

                                                                                        (100)                                               (200 links)
threshold probability of transmission
                                        0.8                                                              0.8


                                        0.6                                                              0.6


                                        0.4                 local                random                  0.4

                                                            small-world          scale-free 2            0.2
                                        0.2
                                                            scale-free 0         scale-free 1
                                        0.0
                                                                                                         0.0
                                              -0.6   -0.4     -0.2   0.0   0.2   0.4   0.6   0.8   1.0         -0.4    -0.2    0.0   0.2     0.4   0.6   0.8   1.0
                                        1.0                                                              1.0


                                        0.8                                             (400)            0.8
                                                                                                                                           (1000 links)
                                        0.6                                                              0.6


                                        0.4                                                              0.4


                                        0.2                                                              0.2


                                        0.0                                                              0.0
                                              -0.6   -0.4     -0.2   0.0   0.2   0.4   0.6   0.8   1.0          -0.4    -0.2   0.0   0.2     0.4   0.6   0.8   1.0

                                                        correlation coefficient between in- and out-degree
                   from: Moslonka-Lefebvre et al. (submitted)
100                                      100



                                             75
                                                      (local)                         75
                                                                                               (sw)
(N of nodes with infection status > 0.01)    50                                       50



                                             25                                       25



                                              0                                        0
                                                  0           25   50    75    100         0          25   50   75   100
          epidemic final size




                                            100                                      100

                                                      (rand)
                                             75                                       75
                                                                                               (sf2)
                                             50                                       50


                                             25                                       25


                                              0                                        0
                                                  0       25       50    75    100         0          25   50   75   100

                                            100                                      100


                                             75
                                                      (sf0)                           75       (sf1)
                                             50                                       50


                                             25                                       25


                                              0                                        0
                                                  0       25       50    75    100         0          25   50   75   100

                                                                   starting node of the epidemic
2.0                                                          3.0
                                                      local                                             2.5           sw
                                           1.5
across all nodes (+0.01 for sf networks)                                                                2.0
sum at equilibrium of infection status

                                           1.0                                                          1.5
                                                                                                        1.0
                                           0.5
                                                                                                        0.5
                                           0.0                                                          0.0
                                                  0       1         2    3     4         5          6           0               2          4         6          8
                                           3.0                                                           1 .0

                                           2.5          rand                                                         sf2 (log-log)
                                           2.0
                                           1.5                                                           0 .0

                                           1.0
                                           0.5
                                           0.0                                                          -1 .0
                                                                                                                -1              0          1         2          3
                                                  0       2         4    6    8          10    12
                                                                                                            2.0
                                            2.0

                                            1.5       sf0 (log-log)                                         1.5           sf1 (log-log)
                                            1.0                                                             1.0

                                            0.5                                                             0.5

                                            0.0                                                             0.0

                                           -0.5                                                            -0.5

                                           -1.0                                                            -1.0
                                                  0.0         0.5       1.0        1.5        2.0                   0.0       0.2    0.4       0.6       0.8   1.0

                                                        n of links from starting node                                     n of links from starting node
Correlation of epidemic final size with out-degree of
 starting node increases with network connectivity




                         N replicates = 100; error bars are St. Dev.;
           different letters show sign. different means at p < 0.05
Conclusions

      1. lower epidemic threshold
    for two-way scale-free networks

 2. importance of the in-out correlation

       3. out-degree as a predictor
          of epidemic final size

4. implications for the horticultural trade
A very short history of ornamental gardens




Thebes, ~1500 BCE    Florence, 16th century   Gardens of Heligan,
                                                17-18th century




  California, ramorum-            California, ramorum-affected
  affected nursery, 2004               urban setting, 2000
Contemporary
 ornamental
    trade
   patterns


 From International
Statistics Flower and
Plants 2004, Institut
  fuer Gartenbau-
   oekonomie der
     Universitaet
      Hannover,
      Germany
Acknowledgements

Jennifer                Richard
Parke,               Baker, CSL
Univ. of                                     Alan
Oregon                                     Inman,   Mike Shaw,
                                           DEFRA    University of
                                                      Reading


                                 Ottmar
                           Holdenrieder,
                              ETHZ, CH
Xiangming Xu,
 East Malling                                       Tom
   Research      Joan Webber,                    Harwood,
                Forest Research,                CEP, Imperial
                   Farnham                        College
References
Dehnen-Schmutz K, Holdenrieder O, Jeger MJ & Pautasso M (2010) Structural change in the international horticultural
industry: some implications for plant health. Scientia Horticulturae 125: 1-15
Harwood TD, Xu XM, Pautasso M, Jeger MJ & Shaw M (2009) Epidemiological risk assessment using linked network
and grid based modelling: Phytophthora ramorum and P. kernoviae in the UK. Ecological Modelling 220: 3353-3361
Jeger MJ & Pautasso M (2008) Comparative epidemiology of zoosporic plant pathogens. European Journal of Plant
Pathology 122: 111-126
MacLeod A, Pautasso M, Jeger MJ & Haines-Young R (2010) Evolution of the international regulation of plant pests and
challenges for future plant health. Food Security 2: 49-70
Moslonka-Lefebvre M, Pautasso M & Jeger MJ (2009) Disease spread in small-size directed networks: epidemic
threshold, correlation between links to and from nodes, and clustering. Journal of Theoretical Biology 260: 402-411
Moslonka-Lefebvre M, Finley A, Dorigatti I, Dehnen-Schmutz K, Harwood T, Jeger MJ, Xu XM, Holdenrieder O &
Pautasso M (2011) Networks in plant epidemiology: from genes to landscapes, countries and continents.
Phytopathology 101: 392-403
Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspectives in Plant Ecology,
Systematics and Evolution 11: 157-189
Pautasso M, Dehnen-Schmutz K, Holdenrieder O, Pietravalle S, Salama N, Jeger MJ, Lange E & Hehl-Lange S (2010)
Plant health and global change – some implications for landscape management. Biological Reviews 85: 729-755
Pautasso M, Moslonka-Lefebvre M & Jeger MJ (2010) The number of links to and from the starting node as a predictor
of epidemic size in small-size directed networks. Ecological Complexity 7: 424-432
Pautasso M, Xu XM, Jeger MJ, Harwood T, Moslonka-Lefebvre M & Pellis L (2010) Disease spread in small-size
directed trade networks: the role of hierarchical categories. Journal of Applied Ecology 47: 1300-1309
Xu XM, Harwood TD, Pautasso M & Jeger MJ (2009) Spatio-temporal analysis of an invasive plant pathogen
(Phytophthora ramorum) in England and Wales. Ecography 32: 504-516

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Models of disease spread in small-size directed networks

  • 1. Plant disease spread and establishment in small-size directed networks Mathieu Moslonka-Lefebvre, Marco Pautasso & Mike Jeger Imperial College London, Silwood Park IEW 10, Geneva, NY - 10 June 2009 Photo: Ottmar Holdenrieder
  • 2. Outline of the talk 1. The relevance of networks for disease epidemiology 2. Case study: Phytophthora ramorum 3. Simulations of disease spread in small-size directed networks 4. Conclusions
  • 3. Disease spread in a globalized world number of passengers per day Hufnagel et al. (2004) Forecast and control of epidemics in a globalized world. PNAS
  • 4. Understanding human mobility patterns Matisoo-Smith et al. (1998) Patterns of prehistoric human mobility in Polynesia indicated by mtDNA from the Pacific rat. PNAS
  • 5. Understanding plant mobility patterns Vendramin et al. (2008) Genetically depauperate but widespread: the case of an emblematic Mediterranean pine. Evolution
  • 6. Plant nurseries as hubs 100 km 2000-2004 Brenn et al. (2008) Community structure of Phialocephala fortinii s. lat. in European tree nurseries, and assessment of the potential of the seedlings as dissemination vehicles. Mycological Research
  • 7. Epidemiology is just one of the many applications of network theory Network pictures from: NATURAL Newman (2003) SIAM Review food webs cell metabolism neural Food web of Little Rock networks Lake, Wisconsin, US ant nests sexual partnerships DISEASE SPREAD family innovation networks Internet flows co-authorship HIV structure railway urban road nets spread electrical networks networks network power grids telephone calls WWW computing airport Internet E-mail committees grids networks software maps patterns TECHNOLOGICAL SOCIAL modified from: Jeger et al. (2007) New Phytologist
  • 8. Outline of the talk 1. The relevance of networks for disease epidemiology 2. Case study: Phytophthora ramorum 3. Simulations of disease spread in small-size directed networks 4. Conclusions
  • 9. from: McKelvey et al. (2007) SOD Science Symposium III
  • 10. P. ramorum Map from www.suddenoakdeath.org confirmations on Kelly, UC-Berkeley the US West Coast vs. national risk Hazard map: Koch & Smith, 3rd SOD Science Symposium (2007)
  • 11. Phytophthora ramorum in England & Wales (2003-2006) 511 nurseries/ 168 historic gardens/ garden centres woodlands 122 85 2003- 46 2003- Jun 2008 Jun 426 2008 Climatic match courtesy of Outbreak maps courtesy of Richard Baker, CSL, UK David Slawson, PHSI, DEFRA, UK
  • 12. Outline of the talk 1. The relevance of networks for disease epidemiology 2. Case study: Phytophthora ramorum 3. Simulations of disease spread in small-size directed networks 4. Conclusions
  • 13. Fraction of population infected (l) as a function of ρ0 uniform degree distribution scale-free network with P(i) ≈ i-3 ρ0 is coincident with R0 for a uniform degree distribution; for a scale-free network, theory says that R0 = ρ0 + [1 + (CV)2], where CV is the coefficient of variation of the degree distribution May (2006) Network structure and the biology of populations. Trends in Ecology & Evolution
  • 14. Simple model of infection spread (e.g. P. ramorum) in a network pt probability of infection transmission pp probability of infection persistence node 1 2 3 4 5 6 7 8 … 100 step 1 step 2 step 3 … step n
  • 15. The four basic types of network structure used SIS Model, 100 Nodes, directed networks, P [i (x, t)] = Σ {p [s] * P [i (y, t-1)] + p [p] * P [i (x, t-1)]} local small- world random scale-free
  • 16. Examples of epidemic development in four kinds of directed networks of small size (at threshold conditions) sum probability of infection across all nodes 1.2 40 1.2 25 local 35 small-world % nodes with probability of infection > 0.01 1.0 1.0 20 30 0.8 0.8 25 15 0.6 20 0.6 10 15 0.4 0.4 10 5 0.2 0.2 5 0.0 0 0.0 0 1 51 101 151 201 1 26 51 76 1.2 80 1.6 60 scale-free 70 random 1.4 1.0 50 1.2 60 40 0.8 1.0 50 0.8 30 0.6 40 0.6 30 20 0.4 0.4 20 10 0.2 0.2 10 0.0 0 0.0 0 1 26 51 76 1 26 51 76 from: Pautasso & Jeger (2008) Ecological Complexity
  • 17. Lower epidemic threshold for scale-free networks with positive correlation between in- and out-degree 1.00 local probability of persistence random 0.75 small-world scale-free (two-way) scale-free (uncorrelated) 0.50 scale-free (one way) 0.25 0.00 0.00 0.25 0.50 0.75 1.00 Epidemic probability of transmission does not develop Epidemic develops modified from: Pautasso & Jeger (2008) Ecological Complexity
  • 18. Lower epidemic threshold for two-way scale-free networks (unless networks are sparsely connected) N replicates = 100; error bars are St. Dev.; different letters show sign. different means at p < 0.05 from: Moslonka-Lefebvre et al. (submitted)
  • 19. 1.0 1.0 (100) (200 links) threshold probability of transmission 0.8 0.8 0.6 0.6 0.4 local random 0.4 small-world scale-free 2 0.2 0.2 scale-free 0 scale-free 1 0.0 0.0 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 1.0 1.0 0.8 (400) 0.8 (1000 links) 0.6 0.6 0.4 0.4 0.2 0.2 0.0 0.0 -0.6 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 -0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0 correlation coefficient between in- and out-degree from: Moslonka-Lefebvre et al. (submitted)
  • 20. 100 100 75 (local) 75 (sw) (N of nodes with infection status > 0.01) 50 50 25 25 0 0 0 25 50 75 100 0 25 50 75 100 epidemic final size 100 100 (rand) 75 75 (sf2) 50 50 25 25 0 0 0 25 50 75 100 0 25 50 75 100 100 100 75 (sf0) 75 (sf1) 50 50 25 25 0 0 0 25 50 75 100 0 25 50 75 100 starting node of the epidemic
  • 21. 2.0 3.0 local 2.5 sw 1.5 across all nodes (+0.01 for sf networks) 2.0 sum at equilibrium of infection status 1.0 1.5 1.0 0.5 0.5 0.0 0.0 0 1 2 3 4 5 6 0 2 4 6 8 3.0 1 .0 2.5 rand sf2 (log-log) 2.0 1.5 0 .0 1.0 0.5 0.0 -1 .0 -1 0 1 2 3 0 2 4 6 8 10 12 2.0 2.0 1.5 sf0 (log-log) 1.5 sf1 (log-log) 1.0 1.0 0.5 0.5 0.0 0.0 -0.5 -0.5 -1.0 -1.0 0.0 0.5 1.0 1.5 2.0 0.0 0.2 0.4 0.6 0.8 1.0 n of links from starting node n of links from starting node
  • 22. Correlation of epidemic final size with out-degree of starting node increases with network connectivity N replicates = 100; error bars are St. Dev.; different letters show sign. different means at p < 0.05
  • 23. Conclusions 1. lower epidemic threshold for two-way scale-free networks 2. importance of the in-out correlation 3. out-degree as a predictor of epidemic final size 4. implications for the horticultural trade
  • 24. A very short history of ornamental gardens Thebes, ~1500 BCE Florence, 16th century Gardens of Heligan, 17-18th century California, ramorum- California, ramorum-affected affected nursery, 2004 urban setting, 2000
  • 25. Contemporary ornamental trade patterns From International Statistics Flower and Plants 2004, Institut fuer Gartenbau- oekonomie der Universitaet Hannover, Germany
  • 26. Acknowledgements Jennifer Richard Parke, Baker, CSL Univ. of Alan Oregon Inman, Mike Shaw, DEFRA University of Reading Ottmar Holdenrieder, ETHZ, CH Xiangming Xu, East Malling Tom Research Joan Webber, Harwood, Forest Research, CEP, Imperial Farnham College
  • 27. References Dehnen-Schmutz K, Holdenrieder O, Jeger MJ & Pautasso M (2010) Structural change in the international horticultural industry: some implications for plant health. Scientia Horticulturae 125: 1-15 Harwood TD, Xu XM, Pautasso M, Jeger MJ & Shaw M (2009) Epidemiological risk assessment using linked network and grid based modelling: Phytophthora ramorum and P. kernoviae in the UK. Ecological Modelling 220: 3353-3361 Jeger MJ & Pautasso M (2008) Comparative epidemiology of zoosporic plant pathogens. European Journal of Plant Pathology 122: 111-126 MacLeod A, Pautasso M, Jeger MJ & Haines-Young R (2010) Evolution of the international regulation of plant pests and challenges for future plant health. Food Security 2: 49-70 Moslonka-Lefebvre M, Pautasso M & Jeger MJ (2009) Disease spread in small-size directed networks: epidemic threshold, correlation between links to and from nodes, and clustering. Journal of Theoretical Biology 260: 402-411 Moslonka-Lefebvre M, Finley A, Dorigatti I, Dehnen-Schmutz K, Harwood T, Jeger MJ, Xu XM, Holdenrieder O & Pautasso M (2011) Networks in plant epidemiology: from genes to landscapes, countries and continents. Phytopathology 101: 392-403 Pautasso M (2009) Geographical genetics and the conservation of forest trees. Perspectives in Plant Ecology, Systematics and Evolution 11: 157-189 Pautasso M, Dehnen-Schmutz K, Holdenrieder O, Pietravalle S, Salama N, Jeger MJ, Lange E & Hehl-Lange S (2010) Plant health and global change – some implications for landscape management. Biological Reviews 85: 729-755 Pautasso M, Moslonka-Lefebvre M & Jeger MJ (2010) The number of links to and from the starting node as a predictor of epidemic size in small-size directed networks. Ecological Complexity 7: 424-432 Pautasso M, Xu XM, Jeger MJ, Harwood T, Moslonka-Lefebvre M & Pellis L (2010) Disease spread in small-size directed trade networks: the role of hierarchical categories. Journal of Applied Ecology 47: 1300-1309 Xu XM, Harwood TD, Pautasso M & Jeger MJ (2009) Spatio-temporal analysis of an invasive plant pathogen (Phytophthora ramorum) in England and Wales. Ecography 32: 504-516