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A Sterility–Mortality Tolerance Trade-Off Leads to Within-Population Variation in Host Tolerance

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Abstract

While experimental studies have demonstrated within-population variation in host tolerance to parasitism, theoretical studies rarely predict for polymorphism to arise. However, most theoretical models do not consider the crucial distinction between tolerance to the effects of infection-induced deaths (mortality tolerance) and tolerance to the parasite-induced reduction in the reproduction of infected hosts (sterility tolerance). While some studies have examined trade-offs between host tolerance and resistance mechanisms, none has considered a correlation within different tolerance mechanisms. We assume that sterility tolerance and mortality tolerance are directly traded-off in a host population subjected to a pathogen and use adaptive dynamics to study their evolutionary behaviour. We find that such a trade-off between the two tolerance strategies can drive the host population to branch into dimorphic strains, leading to coexistence of strains with sterile hosts that have low mortality and fully fertile with high mortality rates. Further, we find that a wider range of trade-off shapes allows branching at intermediate- or high-infected population size. Our other significant finding is that sterility tolerance is maximised (and mortality tolerance minimised) at an intermediate disease-induced mortality rate. Additionally, evolution entirely reverses the disease prevalence pattern corresponding to the recovery rate, compared to when no strategies evolve. We provide novel predictions on the evolutionary behaviour of two tolerance strategies concerning such a trade-off.

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References

  • Abbate JL, Kada S, Lion S (2015) Beyond mortality: sterility as a neglected component of parasite virulence. PLoS Pathog 11(12):e1005229

    Article  Google Scholar 

  • Agrawal AA, Conner JK, Stinchcombe JR (2004) Evolution of plant resistance and tolerance to frost damage. Ecol Lett 7(12):1199–1208

    Article  Google Scholar 

  • Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Philos Trans R Soc B: Biol Sci 291(1054):451–524

    Google Scholar 

  • Antonovics J, Thrall PH (1994) The cost of resistance and the maintenance of genetic polymorphism in host-pathogen systems. Proc R Soc B: Biol Sci 257(1349):105–110

    Article  Google Scholar 

  • Bartlett LJ, Boots M (2021) The central role of host reproduction in determining the evolution of virulence in spatially structured populations. J Theor Biol 523:110717

    Article  MathSciNet  MATH  Google Scholar 

  • Baucom RS, Mauricio R (2008) Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive. Evol Int J Org Evol 62(11):2842–2854

    Article  Google Scholar 

  • Berec L, Maxin D (2012) Double impact of sterilizing pathogens: added value of increased life expectancy on pest control effectiveness. J Math Biol 64(7):1281–1311

    Article  MathSciNet  MATH  Google Scholar 

  • Best A, White A, Boots M (2008) Maintenance of host variation in tolerance to pathogens and parasites. Proc Natl Acad Sci U S A 105(52):20786–20791

    Article  Google Scholar 

  • Best A, White A, Boots M (2010a) Resistance is futile but tolerance can explain why parasites do not always castrate their hosts. Evol Int J Org Evol 64(2):348–357

  • Best A, White A, Kisdi E, Antonovics J, Brockhurst M, Boots M (2010b) The evolution of host-parasite range. Am Nat 176(1):63–71

  • Best A, White A, Boots M (2014) The coevolutionary implications of host tolerance. Evolution 68(5):1426–1435

    Article  Google Scholar 

  • Best A, White A, Boots M (2017) The evolution of host defence when parasites impact reproduction. Evol Ecol Res 18:393–409

    Google Scholar 

  • Blanchet S, Rey O, Loot G (2010) Evidence for host variation in parasite tolerance in a wild fish population. Evol Ecol 24(5):1129–1139

    Article  Google Scholar 

  • Bonds MH (2006) Host life-history strategy explains pathogen-induced sterility. Am Nat 168(3):281–293

    Article  Google Scholar 

  • Boots M, Bowers RG (1999) Three mechanisms of host resistance to microparasites-avoidance, recovery and tolerance-show different evolutionary dynamics. J Theor Biol 201(1):13–23

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Boots M, Best A, Miller MR, White A (2009) The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philos Trans R Soc B: Biol Sci 364(1513):27–36

    Article  Google Scholar 

  • Boots M, White A, Best A, Bowers R (2012) The importance of who infects whom: the evolution of diversity in host resistance to infectious disease. Ecol Lett 15(10):1104–1111

    Article  Google Scholar 

  • Bowers RG, Boots M, Begon M (1994) Life-history trade-offs and the evolution of pathogen resistance: competition between host strains. Proc R Soc B: Biol Sci 257(1350):247–253

    Article  Google Scholar 

  • Bowers RG, Hoyle A, White A, Boots M (2005) The geometric theory of adaptive evolution: trade-off and invasion plots. J Theor Biol 233(3):363–377

    Article  MathSciNet  MATH  Google Scholar 

  • Budischak SA, Cressler CE (2018) Fueling defense: effects of resources on the ecology and evolution of tolerance to parasite infection. Front Immunol 9:2453

    Article  Google Scholar 

  • Carval D, Ferriere R (2010) A unified model for the coevolution of resistance, tolerance, and virulence. Evol Int J Org Evol 64(10):2988–3009

    Google Scholar 

  • Donnelly R, White A, Boots M (2015) The epidemiological feedbacks critical to the evolution of host immunity. J Evol Biol 28(11):2042–2053

    Article  Google Scholar 

  • Eshel I (1983) Evolutionary and continuous stability. J Theor Biol 103(1):99–111

    Article  MathSciNet  Google Scholar 

  • Feore SM, Bennett M, Chantrey J, Jones T, Baxb D, Begon M (1997) The effect of cowpox virus infection on fecundity in bank voles and wood mice. Proc R Soc B: Biol Sci 264(1387):1457–1461

    Article  Google Scholar 

  • Ferris C, Best A (2019) The effect of temporal fluctuations on the evolution of host tolerance to parasitism. Theor Popul Biol 130:182–190

    Article  MATH  Google Scholar 

  • Fineblum WL, Rausher MD (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377(6549):517–520

    Article  Google Scholar 

  • Gandon S, Agnew P, Michalakis Y (2002) Coevolution between parasite virulence and host life-history traits. Am Nat 160(3):374–388

    Article  Google Scholar 

  • Geritz SA, Metz JA, Kisdi É, Meszéna G (1997) Dynamics of adaptation and evolutionary branching. Phys Rev Lett 78(10):2024

    Article  Google Scholar 

  • Geritz SA, Mesze G, Metz JA et al (1998) Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree. Evol Ecol 12(1):35–57

    Article  Google Scholar 

  • Goulson D, Cory JS (1995) Responses of mamestra brassicae (Lepidoptera: Noctuidae) to crowding: interactions with disease resistance, colour phase and growth. Oecologia 104(4):416–423

    Article  Google Scholar 

  • Hochberg M, Michalakis Y, De Meeus T (1992) Parasitism as a constraint on the rate of life-history evolution. J Evol Biol 5(3):491–504

    Article  Google Scholar 

  • Hoyle A, Best A, Bowers R (2012) Evolution of host resistance towards pathogen exclusion: the role of predators. Evol Ecol Res 14(2):125–146

    Google Scholar 

  • Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17(8):363–368

    Article  Google Scholar 

  • Janoušková E, Berec L (2018) Host-pathogen dynamics under sterilizing pathogens and fecundity-longevity trade-off in hosts. J Theor Biol 450:76–85

    Article  MathSciNet  MATH  Google Scholar 

  • Janoušková E, Berec L (2020) Fecundity-longevity trade-off, vertical transmission, and evolution of virulence in sterilizing pathogens. Am Nat 195(1):95–106

    Article  Google Scholar 

  • Jensen KH, Little T, Skorping A, Ebert D (2006) Empirical support for optimal virulence in a castrating parasite. PLoS Biol 4(7):e197

    Article  Google Scholar 

  • Kada S, Lion S (2015) Superinfection and the coevolution of parasite virulence and host recovery. J Evol Biol 28(12):2285–2299

    Article  Google Scholar 

  • Kisdi É (2006) Trade-off geometries and the adaptive dynamics of two co-evolving species. Evol Ecol Res 8(6):959–973

    Google Scholar 

  • Koskela T, Puustinen S, Salonen V, Mutikainen P (2002) Resistance and tolerance in a host plant-holoparasitic plant interaction: Genetic variation and costs. Evolution 56(5):899–908

    Google Scholar 

  • Krist AC (2001) Variation in fecundity among populations of snails is predicted by prevalence of castrating parasites. Evol Ecol Res 3(2):191–197

    Google Scholar 

  • Kutzer MA, Kurtz J, Armitage SA (2018) Genotype and diet affect resistance, survival, and fecundity but not fecundity tolerance. J Evol Biol 31(1):159–171

    Article  Google Scholar 

  • Lafferty KD, Kuris AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends Parasitol 25(12):564–572

    Article  Google Scholar 

  • Leventhal GE, Dünner RP, Barribeau SM (2014) Delayed virulence and limited costs promote fecundity compensation upon infection. Am Nat 183(4):480–493

    Article  Google Scholar 

  • Lindsey E, Mehta M, Dhulipala V, Oberhauser K, Altizer S (2009) Crowding and disease: effects of host density on response to infection in a butterfly-parasite interaction. Ecol Entomol 34(5):551–561

    Article  Google Scholar 

  • Mauricio R, Rausher MD, Burdick DS (1997) Variation in the defense strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78(5):1301–1311

    Article  Google Scholar 

  • Metz J, Geritz S, Meszéna G (1995) Adaptive dynamics, a geometrical study of the consequences of nearly faithful reproduction. Inst Appl Syst Anal Int 42

  • Mikaberidze A, McDonald BA (2020) A tradeoff between tolerance and resistance to a major fungal pathogen in elite wheat cultivars. New Phytol 226(3):879–890

    Article  Google Scholar 

  • Miller MR (2006) Theoretical models for the evolution and ecological dynamics of host-parasite systems. Ph.D. Thesis, University of Sheffield

  • Miller M, White A, Boots M (2005) The evolution of host resistance: tolerance and control as distinct strategies. J Theor Biol 236(2):198–207

    Article  MathSciNet  MATH  Google Scholar 

  • Miller MR, White A, Boots M (2007) Host life span and the evolution of resistance characteristics. Evolution 61(1):2–14

    Article  Google Scholar 

  • Montes N, Alonso-Blanco C, García-Arenal F (2019) Cucumber mosaic virus infection as a potential selective pressure on Arabidopsis thaliana populations. PLoS Pathog 15(5):e1007810

    Article  Google Scholar 

  • Montes N, Vijayan V, Pagán I (2020) Trade-offs between host tolerances to different pathogens in plant-virus interactions. Virus Evol 6(1):veaa019

    Article  Google Scholar 

  • Pagán I, García-Arenal F (2018) Tolerance to plant pathogens: theory and experimental evidence. Int J Mol Sci 19(3):810

    Article  Google Scholar 

  • Pagán I, Alonso-Blanco C, García-Arenal F (2007) The relationship of within-host multiplication and virulence in a plant-virus system. PLoS ONE 2(8):e786

    Article  Google Scholar 

  • Pagán I, Alonso-Blanco C, García-Arenal F (2008) Host responses in life-history traits and tolerance to virus infection in Arabidopsis thaliana. PLoS Pathog 4(8):e1000124

    Article  Google Scholar 

  • Parker BJ, Garcia JR, Gerardo NM (2014) Genetic variation in resistance and fecundity tolerance in a natural host-pathogen interaction. Evolution 68(8):2421–2429

    Google Scholar 

  • Pike VL, Ford SA, King KC, Rafaluk-Mohr C (2019) Fecundity compensation is dependent on the generalized stress response in a nematode host. Ecol Evol 9(20):11957–11961

    Article  Google Scholar 

  • Pilson D (2000) The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in brassica rapa. Evol Ecol 14(4):457–489

    Article  Google Scholar 

  • Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318(5851):812–814

    Article  Google Scholar 

  • Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc B: Biol Sci 364(1513):37–49

    Article  Google Scholar 

  • Rafaluk-Mohr C, Gerth M, Sealey JE, Ekroth AK, Aboobaker AA, Kloock A, King KC (2022) Microbial protection favors parasite tolerance and alters host-parasite coevolutionary dynamics. Curr Biol 32:1593–1598

    Article  Google Scholar 

  • Reilly JR, Hajek AE (2008) Density-dependent resistance of the gypsy moth Lymantria dispar to its nucleopolyhedrovirus, and the consequences for population dynamics. Oecologia 154(4):691–701

    Article  Google Scholar 

  • Restif O, Koella JC (2003) Shared control of epidemiological traits in a coevolutionary model of host-parasite interactions. Am Nat 161(6):827–836

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Roy B, Kirchner J (2000) Evolutionary dynamics of pathogen resistance and tolerance. Evolution 54(1):51–63

    Google Scholar 

  • Singh P, Best A (2021) Simultaneous evolution of host resistance and tolerance to parasitism. J Evol Biol 34:1932–1943

    Article  Google Scholar 

  • Sloan D, Giraud T, Hood M (2008) Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts. J Evol Biol 21(6):1544–1554

    Article  Google Scholar 

  • Thrall PH, Antonovics J, Wilson WG (1998) Allocation to sexual versus nonsexual disease transmission. Am Nat 151(1):29–45

    Article  Google Scholar 

  • Tiffin P, Rausher MD (1999) Genetic constraints and selection acting on tolerance to herbivory in the common morning glory Ipomoea purpurea. Am Nat 154(6):700–716

    Article  Google Scholar 

  • Toor J, Best A (2015) The evolution of host resistance to disease in the presence of predators. J Theor Biol 365:104–111

    Article  MathSciNet  MATH  Google Scholar 

  • Vale P, Little T (2012) Fecundity compensation and tolerance to a sterilizing pathogen in daphnia. J Evol Biol 25(9):1888–1896

    Article  Google Scholar 

  • Vijayan V, López-González S, Sánchez F, Ponz F, Pagán I (2017) Virulence evolution of a sterilizing plant virus: tuning multiplication and resource exploitation. Virus Evol 3(2):vex033

    Article  Google Scholar 

  • Vitale C, Best A (2019) The paradox of tolerance: parasite extinction due to the evolution of host defence. J Theor Biol 474:78–87

    Article  MathSciNet  MATH  Google Scholar 

  • Willink B, Svensson EI (2017) Intra-and intersexual differences in parasite resistance and female fitness tolerance in a polymorphic insect. Proc R Soc B: Biol Sci 284(1847):20162407

    Article  Google Scholar 

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Acknowledgements

We thank Charlotte Rafaluk-Mohr for providing biological insights and feedback on an earlier version of the manuscript.

Funding

P. Singh is funded by the University of Sheffield Faculty of Science University Post Graduate Research Committee (UPGRC) Fee Scholarship.

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  1. School of Mathematics and Statistics, University of Sheffield, Sheffield, S3 7RH, UK

    Prerna Singh & Alex Best

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  1. Prerna Singh
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  2. Alex Best
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PS led the design of the study, carried out the evolutionary analysis and numerical simulations, and drafted the manuscript. AB helped design the study and helped draft the manuscript.

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Correspondence to Prerna Singh.

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Singh, P., Best, A. A Sterility–Mortality Tolerance Trade-Off Leads to Within-Population Variation in Host Tolerance. Bull Math Biol 85, 16 (2023). https://doi.org/10.1007/s11538-023-01119-6

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