Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Shoaling guppies evade predation but have deadlier parasites

Nature Ecology & Evolution volume 6, pages 945–954 (2022)Cite this article

Subjects

Abstract

Parasites exploit hosts to replicate and transmit, but overexploitation kills both host and parasite. Predators may shift this cost–benefit balance by consuming infected hosts or changing host behaviour, but the strength of these effects remains unclear. Here we use field and lab data on Trinidadian guppies and their Gyrodactylus spp. parasites to show how differential predation pressure influences parasite virulence and transmission. We use an experimentally demonstrated virulence–transmission trade-off to parametrize a mathematical model in which host shoaling (as a means of anti-predator defence), increases contact rates and selects for higher virulence. Then we validate model predictions by collecting parasites from wild, Trinidadian populations; parasites from high-predation populations were more virulent in common gardens than those from low-predation populations. Broadly, our results indicate that reduced social contact selects against parasite virulence.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Predators alter selection on virulence through consumptive and non-consumptive pathways.
Fig. 2: Natural guppy populations differ in predation, driving evolutionary divergence in shoaling rate.
Fig. 3: Infection intensity links transmission rate and virulence with a stabilizing trade-off.
Fig. 4: Predation drives increased shoaling rate and virulence in the eco-coevolutionary model.
Fig. 5: Predation increases shoaling rate and thus selects for higher virulence.

Similar content being viewed by others

Data availability

The data is available at https://doi.org/10.5061/dryad.k3j9kd59h.

Code availability

The code is available at https://doi.org/10.5061/dryad.k3j9kd59h.

References

  1. Everard, M., Johnston, P., Santillo, D. & Staddon, C. The role of ecosystems in mitigation and management of Covid-19 and other zoonoses. Environ. Sci. Policy 111, 7–17 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. J. Evolut. Biol. 22, 245–259 (2009).

    Article  CAS  Google Scholar 

  3. Cressler, C. E., McLeod, D. V., Rozins, C., Van Den Hoogen, J. & Day, T. The adaptive evolution of virulence: a review of theoretical predictions and empirical tests. Parasitology 143, 915–930 (2016).

    Article  PubMed  Google Scholar 

  4. Acevedo, M. A., Dillemuth, F. P., Flick, A. J., Faldyn, M. J. & Elderd, B. D. Virulence‐driven trade‐offs in disease transmission: a meta‐analysis. Evolution 73, 636–647 (2019).

    Article  PubMed  Google Scholar 

  5. Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).

    Article  PubMed  Google Scholar 

  6. McKay, B., Ebell, M., Dale, A. P., Shen, Y. & Handel, A. Virulence-mediated infectiousness and activity trade-offs and their impact on transmission potential of influenza patients. Proc. R. Soc. B 287, 20200496 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bonneaud, C. et al. Experimental evidence for stabilizing selection on virulence in a bacterial pathogen. Evol. Lett. 4, 491–501 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  8. De Roode, J. C., Yates, A. J. & Altizer, S. Virulence–transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489–7494 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17441–17446 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Choo, K., Williams, P. D. & Day, T. Host mortality, predation and the evolution of parasite virulence. Ecol. Lett. 6, 310–315 (2003).

    Article  Google Scholar 

  11. Williams, P. D. & Day, T. Interactions between sources of mortality and the evolution of parasite virulence. Proc. R. Soc. B 268, 2331–2337 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gandon, S., Jansen, V. A. & Van Baalen, M. Host life history and the evolution of parasite virulence. Evolution 55, 1056–1062 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Prado, F., Sheih, A., West, J. D. & Kerr, B. Coevolutionary cycling of host sociality and pathogen virulence in contact networks. J. Theor. Biol. 261, 561–569 (2009).

    Article  PubMed  Google Scholar 

  14. Herre, E. A. Population structure and the evolution of virulence in nematode parasites of fig wasps. Science 259, 1442–1445 (1993).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Alizon, S., de Roode, J. C. & Michalakis, Y. Multiple infections and the evolution of virulence. Ecol. Lett. 16, 556–567 (2013).

    Article  PubMed  Google Scholar 

  17. Bull, J. J. & Lauring, A. S. Theory and empiricism in virulence evolution. PLoS Pathog. 10, e1004387 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  18. Brown, S. P., Hochberg, M. E. & Grenfell, B. T. Does multiple infection select for raised virulence? Trends Microbiol. 10, 401–405 (2002).

    Article  CAS  PubMed  Google Scholar 

  19. Peacor, S. D. & Werner, E. E. The contribution of trait-mediated indirect effects to the net effects of a predator. Proc. Natl Acad. Sci. USA 98, 3904–3908 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Seppälä, O., Karvonen, A. & Valtonen, E. T. Shoaling behaviour of fish under parasitism and predation risk. Anim. Behav. 75, 145–150 (2008).

    Article  Google Scholar 

  21. Lopez, L. K. & Duffy, M. A. Mechanisms by which predators mediate host–parasite interactions in aquatic systems. Trends Parasitol. 37, 890–906 (2021).

    Article  CAS  PubMed  Google Scholar 

  22. Rigby, M. C. & Jokela, J. Predator avoidance and immune defence: costs and trade-offs in snails. Proc. R. Soc. B 267, 171–176 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Krause, J., Ruxton, G. D., Ruxton, G. & Ruxton, I. G. Living in Groups (Oxford Univ. Press, 2002).

  24. Godin, J.-G. J. Antipredator function of shoaling in teleost fishes: a selective review. Nat. Can. 113, 241–250 (1986).

    Google Scholar 

  25. Gandon, S., van Baalen, M. & Jansen, V. A. The evolution of parasite virulence, superinfection, and host resistance. Am. Nat. 159, 658–669 (2002).

    Article  PubMed  Google Scholar 

  26. Magurran, A. E. Evolutionary Ecology: The Trinidadian Guppy (Oxford Univ. Press, 2005).

  27. Magurran, A. E. & Seghers, B. H. Variation in schooling and aggression amongst guppy (Poecilia reticulata) populations in Trinidad. Behaviour 118, 214–234 (1991).

    Article  Google Scholar 

  28. Seghers, B. H. & Magurran, A. E. Predator inspection behaviour covaries with schooling tendency amongst wild guppy, Poecilia reticulata, populations in Trinidad. Behaviour 128, 121–134 (1994).

    Article  Google Scholar 

  29. Huizinga, M., Ghalambor, C. & Reznick, D. The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata. J. Evolut. Biol. 22, 1860–1866 (2009).

    Article  CAS  Google Scholar 

  30. Stephenson, J. F., Van Oosterhout, C., Mohammed, R. S. & Cable, J. Parasites of Trinidadian guppies: evidence for sex‐ and age‐specific trait‐mediated indirect effects of predators. Ecology 96, 489–498 (2015).

    Article  PubMed  Google Scholar 

  31. Richards, E. L., Van Oosterhout, C. & Cable, J. Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS ONE 5, e13285 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Johnson, M. B., Lafferty, K. D., Van Oosterhout, C. & Cable, J. Parasite transmission in social interacting hosts: monogenean epidemics in guppies. PLoS ONE https://doi.org/10.1371/journal.pone.0022634 (2011).

  33. Gotanda, K. M. et al. Adding parasites to the guppy-predation story: insights from field surveys. Oecologia 172, 155–166 (2013).

    Article  PubMed  Google Scholar 

  34. Fraser, B. A., Ramnarine, I. W. & Neff, B. D. Temporal variation at the MHC class IIB in wild populations of the guppy (Poecilia reticulata). Evolution 64, 2086–2096 (2010).

    PubMed  Google Scholar 

  35. Stephenson, J. F. et al. Host heterogeneity affects both parasite transmission to and fitness on subsequent hosts. Philos. Trans. R. Soc. B 372, 20160093 (2017).

    Article  Google Scholar 

  36. Cable, J. & Van Oosterhout, C. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. Int. J. Parasitol. 37, 1449–1458 (2007).

    Article  CAS  PubMed  Google Scholar 

  37. Reznick, D. N., Butler, M. J. IV, Rodd, F. H. & Ross, P. Life‐history evolution in guppies (Poecilia reticulata) 6. Differential mortality as a mechanism for natural selection. Evolution 50, 1651–1660 (1996).

    PubMed  Google Scholar 

  38. Bonds, M. H., Keenan, D. C., Leidner, A. J. & Rohani, P. Higher disease prevalence can induce greater sociality: a game theoretic coevolutionary model. Evolution 59, 1859–1866 (2005).

    Article  PubMed  Google Scholar 

  39. Kerr, B., Neuhauser, C., Bohannan, B. J. & Dean, A. M. Local migration promotes competitive restraint in a host–pathogen ‘tragedy of the commons’. Nature 442, 75–78 (2006).

    Article  CAS  PubMed  Google Scholar 

  40. Boots, M. & Sasaki, A. ‘Small worlds’ and the evolution of virulence: infection occurs locally and at a distance. Proc. R. Soc. B 266, 1933–1938 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  42. Dargent, F., Rolshausen, G., Hendry, A., Scott, M. & Fussmann, G. Parting ways: parasite release in nature leads to sex‐specific evolution of defence. J. Evolut. Biol. 29, 23–34 (2016).

    Article  CAS  Google Scholar 

  43. Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990).

    Article  Google Scholar 

  44. Stephenson, J. F., van Oosterhout, C. & Cable, J. Pace of life, predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance. Biol. Lett. 11, 20150806 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stephenson, J. F., Stevens, M., Troscianko, J. & Jokela, J. The size, symmetry, and color saturation of a male guppy’s ornaments forecast his resistance to parasites. Am. Naturalist 196, 597–608 (2020).

    Article  Google Scholar 

  46. Godin, J.-G. J. & McDonough, H. E. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav. Ecol. 14, 194–200 (2003).

    Article  Google Scholar 

  47. Van Oosterhout, C., Harris, P. & Cable, J. Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae). Biol. J. Linn. Soc. 79, 645–651 (2003).

    Article  Google Scholar 

  48. Hawley, D. M., Gibson, A. K., Townsend, A. K., Craft, M. E. & Stephenson, J. F. Bidirectional interactions between host social behaviour and parasites arise through ecological and evolutionary processes. Parasitology 148, 274–288 (2020).

    Article  PubMed  Google Scholar 

  49. Janecka, M. J., Rovenolt, F. & Stephenson, J. F. How does host social behavior drive parasite non-selective evolution from the within-host to the landscape-scale? Behav. Ecol. Sociobiol. 75, 1–20 (2021).

    Article  Google Scholar 

  50. Tao, H., Li, L., White, M. C., Steel, J. & Lowen, A. C. Influenza A virus coinfection through transmission can support high levels of reassortment. J. Virol. 89, 8453–8461 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Eshel, I. Evolutionary and continuous stability. J. Theor. Biol. 103, 99–111 (1983).

    Article  Google Scholar 

  52. Hurford, A., Cownden, D. & Day, T. Next-generation tools for evolutionary invasion analyses. J. R. Soc. Interface 7, 561–571 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Leimar, O. Multidimensional convergence stability. Evolut. Ecol. Res. 11, 191–208 (2009).

    Google Scholar 

  54. Reznick, D., Bryant, M. & Holmes, D. The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol. 4, e7 (2005).

    Article  PubMed Central  Google Scholar 

  55. Stephenson, J. F. Parasite-induced plasticity in host social behaviour depends on sex and susceptibility. Biol. Lett. https://doi.org/10.1098/rsbl.2019.0557 (2019).

  56. Lopez, S. Acquired resistance affects male sexual display and female choice in guppies. Proc. R. Soc. B 265, 717–723 (1998).

    Article  Google Scholar 

  57. van Oosterhout, C. et al. Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int. J. Parasitol. 37, 805–812 (2007).

    Article  PubMed  Google Scholar 

  58. Pérez-Jvostov, F., Hendry, A. P., Fussmann, G. F. & Scott, M. E. Are host–parasite interactions influenced by adaptation to predators? A test with guppies and Gyrodactylus in experimental stream channels. Oecologia 170, 77–88 (2012).

    Article  PubMed  Google Scholar 

  59. Eiben, A. E. & Smith, J. E. Introduction to Evolutionary Computing (Springer, 2003).

  60. Carnell, R. lhs: Latin hypercube samples v.1.1.1 (R-Project, 2020).

  61. Iooss, B., Da Veiga, S., Janon, A. & Pujol, G. Sensitivity: Global sensitivity analysis of model outputs v.1.25.0 (R-Project, 2021).

  62. Wright, D. & Krause, J. Repeated measures of shoaling tendency in zebrafish (Danio rerio) and other small teleost fishes. Nat. Protoc. 1, 1828–1831 (2006).

    Article  CAS  PubMed  Google Scholar 

  63. Friard, O. & Gamba, M. BORIS: a free, versatile open‐source event‐logging software for video/audio coding and live observations. Methods Ecol. Evol. 7, 1325–1330 (2016).

    Article  Google Scholar 

  64. Griffiths, S. W. & Magurran, A. E. Sex and schooling behaviour in the Trinidadian guppy. Anim. Behav. 56, 689–693 (1998).

    Article  CAS  PubMed  Google Scholar 

  65. Magurran, A., Seghers, B., Carvalho, G. & Shaw, P. Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: evidence for the evolution of anti-predator behaviour in the wild. Proc. R. Soc. B 248, 117–122 (1992).

    Article  Google Scholar 

  66. Sievers, C. et al. Reasons for the invasive success of a guppy (Poecilia reticulata) population in Trinidad. PLoS ONE 7, e38404 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mohammed, R. S. et al. Parasite diversity and ecology in a model species, the guppy (Poecilia reticulata) in Trinidad. R. Soc. Open Sci. 7, 191112 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Lyles, A. M. Genetic Variation and Susceptibility to Parasites: Poeclia reticulata Infected with Gyrodactylus turnbulli. PhD dissertation, Princeton Univ. (1990).

  69. Fraser, B. A. & Neff, B. D. Parasite mediated homogenizing selection at the MHC in guppies. Genetica 138, 273 (2010).

    Article  CAS  PubMed  Google Scholar 

  70. Reznick, D. & Endler, J. A. The impact of predation on life history evolution in Trinidadian guppies (Poecilia reticulata). Evolution 36, 160–177 (1982).

    PubMed  Google Scholar 

  71. El‐Sabaawi, R. W. et al. Assessing the effects of guppy life history evolution on nutrient recycling: from experiments to the field. Freshw. Biol. 60, 590–601 (2015).

    Article  Google Scholar 

  72. Liley, N. & Luyten, P. Geographic variation in the sexual behaviour of the guppy, Poecilia reticulata (Peters). Behaviour 95, 164–179 (1985).

    Article  Google Scholar 

  73. Reznick, D. N. et al. Eco-evolutionary feedbacks predict the time course of rapid life-history evolution. Am. Nat. 194, 671–692 (2019).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank M. Ramlal, D. Reznick and E. Rudzki for assistance with fieldwork. E. Calcaterra, L. Colgan, J. Jokela, M. Sackett and N. Tardent provided technical assistance with parasite genotyping. J. Jokela, A. McKay, C. van Oosterhout, M. Turcotte, K. A. Young and three anonymous reviewers made useful comments on an earlier version of this manuscript. National Science Foundation Division of Environmental Biology number 2010826 (J.C.W.), National Science Foundation Division of Environmental Biology number 2010741 (M.J.J.), National Science Foundation Division of Graduate Education number 1747452 (F.R.) and University of Pittsburgh Central Research Development Fund (J.F.S.) provided funding.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA

    Jason C. Walsman, Mary J. Janecka, David R. Clark, Rachael D. Kramp, Faith Rovenolt, Regina Patrick & Jessica F. Stephenson

  2. Department of Life Sciences, University of the West Indies, St. Augustine, Trinidad and Tobago

    Ryan S. Mohammed

  3. Biology Department, Thompson Biology Lab, Williams College, Williamstown, MA, USA

    Ryan S. Mohammed

  4. Evolutionary Biology Group, Faculty of Biology, Adam Mickiewicz University, Poznań, Poland

    Mateusz Konczal

  5. School of Biological Sciences, University of Nebraska, Lincoln, NE, USA

    Clayton E. Cressler

Authors
  1. Jason C. Walsman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mary J. Janecka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David R. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rachael D. Kramp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Faith Rovenolt
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Regina Patrick
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ryan S. Mohammed
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mateusz Konczal
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Clayton E. Cressler
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jessica F. Stephenson
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: J.F.S. and J.C.W. Theoretical modelling: J.C.W., C.E.C. and J.F.S. Data collection from literature: F.R. Sensitivity analysis: J.C.W. and F.R. Field collections: M.J.J., D.R.C., R.P. and R.S.M. Laboratory trait measurements: R.P., D.R.C., M.J.J., R.D.K. and J.F.S. Parasite molecular work: M.J.J., R.D.K. and M.K. Parasite genetic analysis: M.J.J. and M.K. Trait data analysis: J.C.W., D.R.C. and J.F.S. Density and prevalence data analysis: J.C.W. Funding acquisition: J.C.W., M.J.J., F.R. and J.F.S. Writing, original draft: J.C.W. and J.F.S. Writing, review and editing: J.C.W., M.J.J., D.R.C., R.D.K., F.R., R.P., R.S.M., M.K., C.E.C. and J.F.S.

Corresponding author

Correspondence to Jason C. Walsman.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Elisa Visher and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

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

Extended data

Extended Data Fig. 1 Flow of information between empirical results (row 1), data uses (row 2), and theory (row 3).

(A) Much of the training data came from our field surveys, previously published surveys, and previously published laboratory data (see Fig. 5f–h for field surveys and see Table 1). (B) With our transmission rate experiment (and previously published data), we established the relationship between intensity and transmission rate (Fig. 3a). We connected these data to those from our line traits experiment, which link intensity and death rate (C; a measure of virulence shown in Fig. 3b). Together, these parameterize the transmission and virulence trade-off as training data (Fig. 3c). (D) The line traits experiment also provided validating data (Fig. 5i,j) on the average virulence and intensity of our four wild populations. (E) All training data, including the trade-off, was used to fit the theoretical model. (F) Once fit, the eco-coevolutionary model predicts where along the trade-off parasites should evolve (Figs. 4, 5d,e), predicting average virulence in the four populations of the validating data. Created with Biorender.com.

Extended Data Fig. 2 Data from field survey of coinfection rates in the wild.

For each site (river + predation regime), we genotyped a subset of worms from a sample of fish hosting more than one worm. We show the percent of infections that were pure (of either parasite species, light-yellow columns) and the total percent of pure infections (mid-blue column is sum of light-yellow columns). We also show the percent of coinfections that were multi-genotype coinfections of one species, the other, or contained both species (light pink columns). The sum of just the light pink columns gives the total rate of coinfection for fish infected with more than 1 worm (dark-purple column). The mid-blue and dark-purple columns must always sum to 100% in every row. We multiply the total coinfection rate (dark-purple; coinfections/infections with > 1) by the percentage of infections that have more than 1 worm to get the final, adjusted coinfection rate (coinfections/infections). See Supplementary Fig. 5 for a graphical example. G.t. = G. turnbulli and G.b. = G. bullatarudis.

Extended Data Fig. 3 Neither selective predation nor variation in host immunity qualitatively alter key model outcomes.

We compared the default model case (squares) to variations with selective predation (circles) or immune variation (triangles). We also compare outcomes with full coevolution at a given predation level (colour; P corresponding to Fig. 5) to outcomes without host evolution (grey). (A) Selective predation led to coevolution of lower shoaling rate. Increased immunity in low-predation populations led to coevolution of somewhat higher shoaling rate while decreased immunity in high-predation populations led to coevolution of somewhat lower shoaling rate. (B) Selective predation led to coevolution of lower virulence. Increased immunity in low-predation populations led to coevolution of higher virulence while decreased immunity in high-predation populations led to coevolution of lower virulence. For all models, increased virulence was driven by increased shoaling rate (compare colour points to grey). (C) Selective predation led to lower coevolutionary prevalence. Increased immunity led to lower coevolutionary prevalence while decreased immunity led to higher. (D) Selective predation led to higher coevolutionary host density. Increased immunity led to higher coevolutionary host density while decreased host density led to lower coevolutionary host density.

Extended Data Fig. 4 Virulence can select for increased shoaling rate.

Hosts can evolve increasing shoaling rate in response to increased virulence, especially at very high virulence (beyond range used in main text). (A) Increasing virulence (and transmissibility along the trade-off) can decrease prevalence. (B) Overall parasite-induced mortality can decrease if prevalence declines sharply enough. This decrease occurs because, while parasites are very virulent, very few hosts are infected and suffering that virulence. (C) At high virulence, increasing virulence can select for higher host shoaling rates. Parameters used: c = 2 used for (A) and (B); P = 0.074 used for (C). All other parameters at default (Table 1).

Extended Data Fig. 5 Host evolution in response to increasing predation causes parasite-induced mortality (red curves) to increase more than predator-induced mortality (black curves).

(A) Without host evolution (shoaling rate, c, set to the green point in Fig. 4 while parasites evolve to some CSS), parasite-induced mortality declines with predation while predator-induced mortality increases. Death from background sources (d, grey line) does not change. (B) This trend is similar for a higher c (set to high, blue point in Fig. 4). (C) When hosts evolve increasing c with increasing predation (coCSS curve connecting green and blue points in Fig. 4), parasite-induced mortality increases more than predator-induced mortality. This pattern is due to host evolution and is qualitatively unchanged if hosts evolve but parasites do not.

Supplementary information

Supplementary Information

Supplementary Note, Figs. 1–5 and Tables 1–2.

Reporting Summary

Peer Review File

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Walsman, J.C., Janecka, M.J., Clark, D.R. et al. Shoaling guppies evade predation but have deadlier parasites. Nat Ecol Evol 6, 945–954 (2022). https://doi.org/10.1038/s41559-022-01772-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-022-01772-5

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing