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Evolutionary dynamics in an SI epidemic model with phenotype-structured susceptible compartment

Abstract

We present an SI epidemic model whereby a continuous structuring variable captures variability in proliferative potential and resistance to infection among susceptible individuals. The occurrence of heritable, spontaneous changes in these phenotypic characteristics and the presence of a fitness trade-off between resistance to infection and proliferative potential are explicitly incorporated into the model. The model comprises an ordinary differential equation for the number of infected individuals that is coupled with a partial integrodifferential equation for the population density function of susceptible individuals through an integral term. The expression for the basic reproduction number \(\mathcal {R}_0\) is derived, the disease-free equilibrium and endemic equilibrium of the model are characterised and a threshold theorem involving \(\mathcal {R}_0\) is proved. Analytical results are integrated with the results of numerical simulations of a calibrated version of the model based on the results of artificial selection experiments in a host-parasite system. The results of our mathematical study disentangle the impact of different evolutionary parameters on the spread of infectious diseases and the consequent phenotypic adaption of susceptible individuals. In particular, these results provide a theoretical basis for the observation that infectious diseases exerting stronger selective pressures on susceptible individuals and being characterised by higher infection rates are more likely to spread. Moreover, our results indicate that heritable, spontaneous phenotypic changes in proliferative potential and resistance to infection can either promote or prevent the spread of infectious diseases depending on the strength of selection acting on susceptible individuals prior to infection. Finally, we demonstrate that, when an endemic equilibrium is established, higher levels of resistance to infection and lower degrees of phenotypic heterogeneity among susceptible individuals are to be expected in the presence of infections which are characterised by lower rates of death and exert stronger selective pressures.

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References

  • Abi Rizk L, Burie J-B, Ducrot A (2021) Asymptotic speed of spread for a nonlocal evolutionary-epidemic system. Discrete Continu Dyn Syst. https://doi.org/10.3934/dcds.2021064

    Article  MathSciNet  MATH  Google Scholar 

  • Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc Lond B Biol Sci 291(1054):451–524. https://doi.org/10.1098/rstb.1981.0005

    Article  Google Scholar 

  • Ardaševa A, Gatenby RA, Anderson ARA, Byrne HM, Maini PK, Lorenzi T (2019) Evolutionary dynamics of competing phenotype-structured populations in periodically fluctuating environments. J Math Biol. https://doi.org/10.1007/s00285-019-01441-5

    Article  MATH  Google Scholar 

  • Ardaševa A, Anderson ARA, Gatenby RA, Byrne HM, Maini PK, Lorenzi T (2020) Comparative study between discrete and continuum models for the evolution of competing phenotype-structured cell populations in dynamical environments. Phys Rev E 102(4):042404

    Google Scholar 

  • Berestycki H, Rossi L (2015) Generalizations and properties of the principal eigenvalue of elliptic operators in unbounded domains. Commun Pure Appl Math 68(6):1014–1065

    MathSciNet  MATH  Google Scholar 

  • Berestycki H, Nirenberg L, Varadhan SRS (1994) The principal eigenvalue and maximum principle for second-order elliptic operators in general domains. Commun Pure Appl Anal 47(1):47–92

    MathSciNet  MATH  Google Scholar 

  • Berezin FA, Shubin MA (1991) The Schroedinger equation. Springer, Berlin

    Google Scholar 

  • Boots M, Haraguchi Y (1999) The evolution of costly resistance in host-parasite systems. Am Nat 153(4):359–370

    Google Scholar 

  • Brauer F (2017) Mathematical epidemiology: past, present, and future. Infect Dis Model 2(2):113–127

    Google Scholar 

  • Burie J-B, Djidjou-Demasse R, Ducrot A (2020a) Asymptotic and transient behaviour for a nonlocal problem arising in population genetics. Eur J Appl Math 31(1):84–110

  • Burie J-B, Djidjou-Demasse R, Ducrot A (2020b) Slow convergence to equilibrium for an evolutionary epidemiology integro-differential system. Discrete Continu Dyn Syst Ser B 25(6):2223

  • Burie J-B, Ducrot A, Griette Q, Richard Q (2020c) Concentration estimates in a multi-host epidemiological model structured by phenotypic traits. J Differ Equ 269(12):11492–11539

  • Busenberg SN, Iannelli M, Thieme HR (1991) Global behavior of an age-structured epidemic model. SIAM J Math Anal 22(4):1065–1080

    MathSciNet  MATH  Google Scholar 

  • Chabas H, Lion S, Nicot A, Meaden S, van Houte S, Moineau S, Wahl LM, Westra ER, Gandon S (2018) Evolutionary emergence of infectious diseases in heterogeneous host populations. PLoS Biol 16(9):e2006738

    Google Scholar 

  • Champagnat N, Ferrière R, Arous G (2002) The canonical equation of adaptive dynamics: a mathematical view. Selection 2(1–2):73–83

    Google Scholar 

  • Champagnat N, Ferrière R, Méléard S (2006) Unifying evolutionary dynamics: from individual stochastic processes to macroscopic models. Theor Popul Biol 69(3):297–321

    MATH  Google Scholar 

  • Chisholm RH, Lorenzi T, Desvillettes L, Hughes BD (2016) Evolutionary dynamics of phenotype-structured populations: from individual-level mechanisms to population-level consequences. Z Angew Math Phys 67(4):1–34

    MathSciNet  MATH  Google Scholar 

  • Dallas T, Holtackers M, Drake JM (2016) Costs of resistance and infection by a generalist pathogen. Ecol Evol 6(6):1737–1744

    Google Scholar 

  • Day T, Proulx SR (2004) A general theory for the evolutionary dynamics of virulence. Am Nat 163(4):E40–E63

    Google Scholar 

  • De Roode JC, Culleton R, Cheesman SJ, Carter R, Read AF (2004) Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc R Soc B 271(1543):1073–1080

    Google Scholar 

  • Djidjou-Demasse R, Ducrot A, Fabre F (2017) Steady state concentration for a phenotypic structured problem modeling the evolutionary epidemiology of spore producing pathogens. Math Models Methods Appl Sci 27(02):385–426

    MathSciNet  MATH  Google Scholar 

  • Festa-Bianchet M (1989) Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). J Anim Ecol 58:785–795

    Google Scholar 

  • Génieys S, Volpert V, Auger P (2006) Adaptive dynamics: modelling Darwin’s divergence principle. C R Biol 329(11):876–879

    Google Scholar 

  • Gomes MGM (2019) On the mathematics of populations. bioRxiv. https://doi.org/10.1101/612366v1.abstract

    Article  Google Scholar 

  • Gomes MGM, Aguas R, Lopes JS, Nunes MC, Rebelo C, Rodrigues P, Struchiner CJ (2012) How host heterogeneity governs tuberculosis reinfection? Proc R Soc B 279(1737):2473–2478

    Google Scholar 

  • Grassly NC, Fraser C (2008) Mathematical models of infectious disease transmission. Nat Rev Microbiol 6(6):477–487

    Google Scholar 

  • Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos Trans R Soc Lond B Biol Sci 346(1317):323–331

    Google Scholar 

  • Hethcote H (2000) The mathematics of infectious diseases. SIAM Rev 42(4):599–653. https://doi.org/10.1137/S0036144500371907

    Article  MathSciNet  MATH  Google Scholar 

  • Huppert A, Katriel G (2013) Mathematical modelling and prediction in infectious disease epidemiology. Clin Microbiol Infect 19(11):999–1005

    Google Scholar 

  • Iannelli M, Pugliese A (2015) An introduction to mathematical population dynamics: along the trail of volterra and lotka, vol 79. Springer, Berlin

    MATH  Google Scholar 

  • Inaba H (1990) Threshold and stability results for an age-structured epidemic model. J Math Biol 28(4):411–434

    MathSciNet  MATH  Google Scholar 

  • Inaba H (2012) On a new perspective of the basic reproduction number in heterogeneous environments. J Math Biol 65(2):309–348

    MathSciNet  MATH  Google Scholar 

  • Inaba H (2017) Age-structured population dynamics in demography and epidemiology. Springer, Berlin

    MATH  Google Scholar 

  • Kermack WO, McKendrick AG (1927) A contribution to the mathematical theory of epidemics. Proc Math Phys Eng Sci 115(772):700–721

    MATH  Google Scholar 

  • Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68(11):1431–1437

    Google Scholar 

  • LeVeque RJ (2007) Finite difference methods for ordinary and partial differential equations: steady-state and time-dependent problems, vol 98, Society for Industrial and Applied Mathematics (SIAM), Philadelphia

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88(1):87–98

    Google Scholar 

  • Lorenzi T, Pouchol C (2020) Asymptotic analysis of selection-mutation models in the presence of multiple fitness peaks. Nonlinearity 33:5791

    MathSciNet  MATH  Google Scholar 

  • Lorenzi T, Chisholm RH, Desvillettes L, Hughes BD (2015) Dissecting the dynamics of epigenetic changes in phenotype-structured populations exposed to fluctuating environments. J Theor Biol 386:166–176

    MathSciNet  MATH  Google Scholar 

  • Lou Y, Zhao X-Q (2011) A reaction–diffusion malaria model with incubation period in the vector population. J Math Biol 62(4):543–568

    MathSciNet  MATH  Google Scholar 

  • Marm Kilpatrick A, Daszak P, Jones MJ, Marra PP, Kramer LD (2006) Host heterogeneity dominates West Nile virus transmission. Proc R Soc B 273(1599):2327–2333

    Google Scholar 

  • Novozhilov AS (2008a) Heterogeneous susceptibles-infectives model: mechanistic derivation of the power law transmission function. arXiv preprint arXiv:0809.1578

  • Novozhilov AS (2008b) On the spread of epidemics in a closed heterogeneous population. Math Biosci 215(2):177–185

    MathSciNet  MATH  Google Scholar 

  • Novozhilov AS (2012) Epidemiological models with parametric heterogeneity: deterministic theory for closed populations. Math Model Nat Phenom 7(3):147–167

    MathSciNet  MATH  Google Scholar 

  • Osnas EE, Dobson AP (2012) Evolution of virulence in heterogeneous host communities under multiple trade-offs. Evolution 66(2):391–401

    Google Scholar 

  • Peng R, Zhao X-Q (2012) A reaction–diffusion SIS epidemic model in a time-periodic environment. Nonlinearity 25(5):1451

    MathSciNet  MATH  Google Scholar 

  • Pugliese A (2011) The role of host population heterogeneity in the evolution of virulence. J Biol Dyn 5(2):104–119. https://doi.org/10.1080/17513758.2010.519404

    Article  MathSciNet  MATH  Google Scholar 

  • Restif O, Koella JC (2004) Concurrent evolution of resistance and tolerance to pathogens. Am Nat 164(4):E90–E102

    Google Scholar 

  • Rivero A, Magaud A, Nicot A, Vézilier J (2011) Energetic cost of insecticide resistance in Culex pipiens mosquitoes. J Med Entomol 48(3):694–700

    Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11(8):317–321

    Google Scholar 

  • Smith HL, Thieme HR (2011) Dynamical systems and population persistence. Springer, Berlin

    MATH  Google Scholar 

  • Stace REA, Stiehl T, Chaplain MAJ, Marciniak-Czochra A, Lorenzi T (2020) Discrete and continuum phenotype-structured models for the evolution of cancer cell populations under chemotherapy. Math Model Nat Phenom 15:14

    MathSciNet  MATH  Google Scholar 

  • Stadler T, Bonhoeffer S (2013) Uncovering epidemiological dynamics in heterogeneous host populations using phylogenetic methods. Philos Trans R Soc Lond B Biol Sci 368(1614):20120198

    Google Scholar 

  • Thieme HR (2009) Spectral bound and reproduction number for infinite-dimensional population structure and time heterogeneity. SIAM J Appl Math 70(1):188–211

    MathSciNet  MATH  Google Scholar 

  • Thompson RN, Brooks-Pollock E (2019) Detection, forecasting and control of infectious disease epidemics: modelling outbreaks in humans, animals and plants. Philos Trans R Soc Lond B Biol Sci 374:20190038

    Google Scholar 

  • Veliov VM, Widder A (2016) Aggregation and asymptotic analysis of an SI-epidemic model for heterogeneous populations. Math Med Biol 33(3):295–318

    MathSciNet  MATH  Google Scholar 

  • Wang W, Zhao X-Q (2011) A nonlocal and time-delayed reaction–diffusion model of dengue transmission. SIAM J Appl Math 71(1):147–168

    MathSciNet  MATH  Google Scholar 

  • Wang W, Zhao X-Q (2012) Basic reproduction numbers for reaction–diffusion epidemic models. SIAM J Appl Dyn Syst 11(4):1652–1673

    MathSciNet  MATH  Google Scholar 

  • Webster JP, Woolhouse MEJ (1999) Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system. Philos Trans R Soc Lond B Biol Sci 266(1417):391–396

    Google Scholar 

  • Woolhouse MEJ (1989) The effect of schistosome infection on the mortality rates of Bulinus globosus and Biomphalaria pfeifferi. Ann Trop Med Parasitol 83(2):137–141

    Google Scholar 

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Acknowledgements

T.L. gratefully acknowledges the hospitality provided by the Department of Mathematics of the Università di Trento during his research stays and support from the MIUR grant “Dipartimenti di Eccellenza 2018-2022” Project nr E11G18000350001.

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Correspondence to Tommaso Lorenzi.

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Lorenzi, T., Pugliese, A., Sensi, M. et al. Evolutionary dynamics in an SI epidemic model with phenotype-structured susceptible compartment. J. Math. Biol. 83, 72 (2021). https://doi.org/10.1007/s00285-021-01703-1

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  • DOI: https://doi.org/10.1007/s00285-021-01703-1

Keywords

  • SI models
  • Mathematical epidemiology
  • Phenotypic heterogeneity
  • Spontaneous phenotypic changes
  • Partial integrodifferential equations

Mathematics Subject Classification

  • 35Q92
  • 35B40
  • 35R09
  • 92D30
  • 35J60