Skip to main content
Log in

The scale of competition impacts parasite virulence evolution

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript


The structure of parasite populations can have important consequences for virulence evolution. Both the scale of competition, whether it is more intense in the within versus between host environment, and the mode of transmission, whether parasites transmit alone or in groups between hosts, influence population structure and can select for changes in virulence.

In a selection experiment, we evolved metapopulations of the spider mite parasite Tetranychus urticae, under local (fixed sampling per host patch) or global (sampling determined by host patch productivity) competition, with either co- (with a female parasite from the same host patch) or random (with parasites from different host patches) transmission. After 33 generations of evolution, the fecundity and virulence of each replicate population was measured.

Females from the ‘local-random’ regime were more virulent with higher fecundity than females from the ‘global-random’ regime. There was no difference in virulence or fecundity between females from the ‘global-random’ or ‘global co-transmission’ selection regimes.

These results show that the scale of competition, and not the type of transmission, impacted virulence evolution for T. urticae. Local competition may maintain higher levels of genetic diversity at the level of the metapopulation. As such, intense local, within-host, competition selected for more productive individuals better able to exploit their environment and be the one to transmit to a new host.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of data

The dataset for this study is available in the Zenodo repository doi.10.5281/zenodo.6784690.


  • Alba JM, Schimmel BC, Glas JJ, Ataide LM, Pappas ML, Villarroel CA, Schuurink RC, Sabelis MW, Kant MR (2015) Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol 205:828–840

    Article  CAS  PubMed  Google Scholar 

  • Alizon S (2013) Parasite co-transmission and the evolutionary epidemiology of virulence. Evolution 67:921–933

    Article  PubMed  Google Scholar 

  • Azandeme-Hounmalon GY, Fellous S, Kreiter S, Fiaboe KK, Subramanian S, Kungu M, Martin T (2014) Dispersal behavior of Tetranychus evansi and T. urticae on tomato at several spatial scales and densities: implications for integrated pest management. PLoS ONE 9:e95071

    Article  PubMed  PubMed Central  Google Scholar 

  • Berngruber TW, Lion S, Gandon S (2013) Evolution of suicide as a defence strategy against pathogens in a spatially structured environment. Ecol Lett 16:446–453

    Article  PubMed  Google Scholar 

  • Boots M, Mealor M (2007) Local interactions select for lower pathogen infectivity. Science 315:1284–1286

    Article  CAS  PubMed  Google Scholar 

  • Buckling A, Brockhurst MA (2008) Kin selection and the evolution of virulence. Heredity 100:484–488

    Article  CAS  PubMed  Google Scholar 

  • Chao L, Hanley KA, Burch CL, Dahlberg C, Turner PE (2000) Kin selection and parasite evolution: Higher and lower virulence with hard and soft selection. Q Rev Biol 75:261–275

    Article  CAS  PubMed  Google Scholar 

  • Coombs D, Gilchrist MA, Ball CL (2007) Evaluating the importance of within- and between-host selection pressures on the evolution of chronic pathogens. Theor Popul Biol 72:576–591

    Article  PubMed  Google Scholar 

  • Debarre F, Gandon S (2011) Evolution in heterogeneous environments: between soft and hard selection. Am Nat 177:E84–97

    Article  PubMed  Google Scholar 

  • Duncan AB, Dusi E, Schrallhammer M, Berendonk T, Kaltz O (2018) Population-level dynamics in experimental mixed infections: evidence for competitive exclusion among bacterial parasites of Paramecium caudatum. Oikos 127:1380–1389

    Article  Google Scholar 

  • Ebert D (1998) Experimental evolution of parasites. Science 282:1432–1435

    Article  CAS  PubMed  Google Scholar 

  • Faria GS, Gardner A, Carazo P (2020) Kin discrimination and demography modulate patterns of sexual conflict. Nat Ecol Evol 4:1141–1148

    Article  PubMed  PubMed Central  Google Scholar 

  • Ford SA, Kao D, Williams D, King KC (2016) Microbe-mediated host defence drives the evolution of reduced pathogen virulence. Nature Communications 7:13430

  • Frank SA (1996) Models of parasite virulence. Q Rev Biol 71:37–78

    Article  CAS  PubMed  Google Scholar 

  • Gallet R, Froissart R, Ravigne V (2018) Experimental demonstration of the impact of hard and soft selection regimes on polymorphism maintenance in spatially heterogeneous environments. Evolution

  • Garbutt J, Bonsall MB, Wright DJ, Raymond B (2011) Antagonistic competition moderates virulence in Bacillus thuringiensis. Ecol Lett 14:765–772

    Article  PubMed  Google Scholar 

  • Gardner A, Arce A, Alpedrinha J (2009) Budding dispersal and the sex ratio. J Evol Biol 22:1036–1045

    Article  CAS  PubMed  Google Scholar 

  • Godinho DP, Rodrigues LR, Lefèvre S, Delteil L, Mira AF, Fragata I, Magalhães S, Duncan AB (2021) Virulence constrains transmission even in the absence of a genetic trade-off. biorRxiv: 2021.10.07.463510

  • Grenfell B, Harwood J (1997) (Meta)population dynamics of infectious diseases. Trends Ecol Evol 12:395–399

    Article  CAS  PubMed  Google Scholar 

  • Griffin AS, West SA, Buckling A (2004) Cooperation and competition in pathogenic bacteria. Nature 430:1024–1027

    Article  CAS  PubMed  Google Scholar 

  • Helle W, Sabelis MW (1985) Spider Mites: Their Biology, Natural Enemies and Control. Elsevier, Amsterdam

  • Kamiya T, Mideo N, Alizon S (2018) Coevolution of virulence and immunosuppression in multiple infections. J Evol Biol 31:995–1005

    Article  PubMed  Google Scholar 

  • Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr B, Neuhauser C, Bohannan BJ, Dean AM (2006) Local migration promotes competitive restraint in a host-pathogen ‘tragedy of the commons’. Nature 442:75–78

    Article  CAS  PubMed  Google Scholar 

  • Kummerli R, Gardner A, West SA, Griffin AS (2009) Limited dispersal, budding dispersal, and cooperation: an experimental study. Evolution 63:939–949

    Article  PubMed  Google Scholar 

  • Li J, Margolies DC (1994) Responses to direct and indirect selection on aerial dispersal behaviour in Tetranychus urticae. Heredity 74:10–22

    Article  Google Scholar 

  • Lion S, Boots M (2010) Are parasites “prudent” in space? Ecol Lett 13:1245–1255

    Article  PubMed  PubMed Central  Google Scholar 

  • Magalon H, Nidelet T, Martin G, Kaltz O (2010) Host growth conditions influence experimental evolution of life-history and virulence of a parasite with vertical and horizontal transmission. Evolution 64:2126–2138

    PubMed  Google Scholar 

  • Messenger SL, Molineux IJ, Bull JJ (1999) Virulence evolution in a virus obeys a trade-off. Proc Roy Soc B: Biol Sci266: 397–404

  • Mideo N, Alizon S, Day M (2008) Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol Evol 23:511–517

    Article  PubMed  Google Scholar 

  • Migeon A, Dorkeld F (2022) Spider Mites Web: a comprehensive database for the Tetranychidae. Available from

  • Mira, A.F., Marques, L.M., Magalh?es, S. & Rodrigues, L.R. (2022). A method to measure the damage caused by cell-sucking herbivores. Methods Mol. Biol., 2494, 299?312.

  • Mitchell R (1973) Growth and population dynamics of a spider mite (Tetranychus urticae K., Acarina: Tetranychidae). Ecology 54:1349–1355

    Article  Google Scholar 

  • Olivieri I, Michalakis Y, Gouyon P-H (1995) Metapopulation genetics and the evolution of dispersal. Am Nat 146:202–228

    Article  Google Scholar 

  • Ravigne V, Dieckmann U, Olivieri I (2009) Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat 174:E141–E169

    Article  PubMed  Google Scholar 

  • Raymond B, West SA, Griffin AS, Bonsall MB (2012) The dynamics of cooperative bacterial virulence in the field. Science 337:85–88

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues LR, Torralba Sáez M, Alpedrinha J, Lefèvre S, Brengues M, Magalhães S, Duncan AB (2021) Consequences of population structure for sex allocation and sexual conflict. J Evol Biol 34:525–536

    Article  Google Scholar 

  • Tien NS, Sabelis MW, Egas M (2015) Inbreeding depression and purging in a haplodiploid: gender-related effects. Heredity 114:327–332

    Article  CAS  PubMed  Google Scholar 

  • Vale PF (2013) Killing them softly: managing pathogen polymorphism and virulence in spatially variable environments. Trends Parasitol 29:417–422

    Article  PubMed  PubMed Central  Google Scholar 

  • Vautrin E, Vavre F (2009) Interactions between vertically transmitted symbionts: cooperation or conflict? Trends Microbiol 17:95–99

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Hogg BN, Hougardy E, Nance AH, Daane KM (2019) Potential competitive outcomes among three solitary larval endoparasitoids as candidate agents for classical biological control of Drosophila suzukii. Biol Control 130:18–26

    Article  Google Scholar 

  • Wild G, Gardner A, West SA (2009) Adaptation and the evolution of parasite virulence in a connected world. Nature 459:983–986

    Article  CAS  PubMed  Google Scholar 

  • Wille P, Boller T, Kaltz O (2002) Mixed inoculation alters infection success of strains of the endophyte Epichloe bromicola on its grass host Bromus erectus. Proc Roy Soc B: Biol Sci 269:397–402

    Article  PubMed  PubMed Central  Google Scholar 

  • Zélé F, Santos I, Olivieri I, Weill M, Duron O, Magalhães S (2018) Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiol Ecol 94, fiy051

Download references


We would like to thank Oliver Kaltz and Giacomo Zilio for very helpful comments and discussion, two anonymous reviewers who provided comments that greatly improved the manuscript and people in the Experimental Evolution of Communities team for stimulating discussion.


This work was funded by a joint grant from the Agence Nationale de la Recherche and the Fundação para a Ciência e a Tecnologia to Isabelle Olivieri and Sara Magalhães (FCT-ANR/BIA- EVF/0013/2012) and an ERC consolidator grant to Sara Magalhães (COMPCON GA 725419). This is ISEM contribution number ISEM 2022-161.

Author information

Authors and Affiliations



ABD conceived of the idea for the experiment and wrote the manuscript. SL and ABD performed the experiment. EL, MV and ABD analysed the data.

Corresponding author

Correspondence to Alison B. Duncan.

Ethics declarations

Conflict of interest

Not applicable.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors consent to publication.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Noël, E., Lefèvre, S., Varoqui, M. et al. The scale of competition impacts parasite virulence evolution. Evol Ecol 37, 153–163 (2023).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: