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Ecology directs host–parasite coevolutionary trajectories across Daphnia–microparasite populations

Nature Ecology & Evolution volume 5, pages 480–486 (2021)Cite this article

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Abstract

Host–parasite interactions often fuel coevolutionary change. However, parasitism is one of a myriad of possible ecological interactions in nature. Biotic (for example, predation) and abiotic (for example, temperature) variation can amplify or dilute parasitism as a selective force on hosts and parasites, driving population variation in (co)evolutionary trajectories. We dissected the relationships between wider ecology and coevolutionary trajectory using 16 ecologically complex Daphnia magna–Pasteuria ramosa ponds seeded with an identical starting host (Daphnia) and parasite (Pasteuria) population. We show, using a time-shift experiment and outdoor population data, how multivariate biotic and abiotic ecological differences between ponds caused coevolutionary divergence. Wider ecology drove variation in host evolution of resistance, but not parasite infectivity; parasites subsequently coevolved in response to the changing complement of host genotypes, such that parasites adapted to historically resistant host genotypes. Parasitism was a stronger interaction for the parasite than for its host, probably because the host is the principal environment and selective force, whereas for hosts, parasite-mediated selection is one of many sources of selection. Our findings reveal the mechanisms through which wider ecology creates coevolutionary hotspots and coldspots in biologically realistic arenas of host–parasite interaction, and sheds light on how the ecological theatre can affect the (co)evolutionary play.

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Fig. 1: Coevolutionary trajectories vary across populations.
Fig. 2: Pairwise ecological differences explain population divergence in coevolutionary trajectory.
Fig. 3: Wider ecology drives coevolution through its effects on host evolution.
Fig. 4: Ecological, epidemiological and coevolutionary relationships across populations.

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Data availability

All data are available on Dryad at https://doi.org/10.5061/dryad.qv9s4mwd6.

Code availability

All companion code is available on Dryad at https://doi.org/10.5061/dryad.qv9s4mwd6. As we are actively researching these datasets, we ask that researchers kindly contact us if they are planning to use the data for reasons other than reproducing the findings of our paper.

References

  1. Paterson, S. et al. Antagonistic coevolution accelerates molecular evolution. Nature 464, 275–278 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Schulte, R. D., Makus, C., Hasert, B., Michiels, N. K. & Schulenburg, H. Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl Acad. Sci. USA 107, 7359–7364 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Koskella, B. & Lively, C. M. Evidence for negative frequency-dependent selection during experimental coevolution of a freshwater snail and a sterilizing trematode. Evolution 63, 2213–2221 (2009).

    Article  PubMed  Google Scholar 

  4. Decaestecker, E. et al. Host–parasite ‘Red Queen’ dynamics archived in pond sediment. Nature 450, 870–873 (2007).

    Article  CAS  PubMed  Google Scholar 

  5. Gómez, P. & Buckling, A. Bacteria–phage antagonistic coevolution in soil. Science 332, 106–109 (2011).

    Article  PubMed  Google Scholar 

  6. Refardt, D. & Ebert, D. Inference of parasite local adaptation using two different fitness components. J. Evol. Biol. 20, 921–929 (2007).

    Article  CAS  PubMed  Google Scholar 

  7. Duffy, M. A., Hall, S. R., Cáceres, C. E. & Ives, A. R. Rapid evolution, seasonality, and the termination of parasite epidemics. Ecology 90, 1441–1448 (2009).

    Article  PubMed  Google Scholar 

  8. Springer, Y. P. Clinical resistance structure and pathogen local adaptation in a serpentine flax–flax rust interaction. Evolution 61, 1812–1822 (2007).

    Article  PubMed  Google Scholar 

  9. Tack, A. J. M., Laine, A.-L., Burdon, J. J., Bissett, A. & Thrall, P. H. Below-ground abiotic and biotic heterogeneity shapes above-ground infection outcomes and spatial divergence in a host–parasite interaction. New Phytol. 207, 1159–1169 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wolinska, J. & King, K. C. Environment can alter selection in host–parasite interactions. Trends Parasitol. 25, 236–244 (2009).

    Article  PubMed  Google Scholar 

  11. Auld, S. K. J. R., Hall, S. R., Ochs, J. H., Sebastian, M. & Duffy, M. A. Predators and patterns of within-host growth can mediate both among-host competition and evolution of transmission potential of parasites. Am. Nat. 184, S77–S90 (2014).

    Article  PubMed  Google Scholar 

  12. Wright, R. C. T., Brockhurst, M. A. & Harrison, E. Ecological conditions determine extinction risk in co-evolving bacteria–phage populations. BMC Evol. Biol. 16, 227 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Duffy, M. A. et al. Ecological context influences epidemic size and parasite-driven evolution. Science 335, 1636–1638 (2012).

    Article  CAS  PubMed  Google Scholar 

  14. Auld, S. K. J. R. & Brand, J. Environmental variation causes different (co) evolutionary routes to the same adaptive destination across parasite populations. Evol. Lett. 1, 245–254 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Su, M. & Boots, M. The impact of resource quality on the evolution of virulence in spatially heterogeneous environments. J. Theor. Biol. 416, 1–7 (2017).

    Article  PubMed  Google Scholar 

  16. Auld, S. K. J. R. & Tinsley, M. C. The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms. Heredity 114, 125–132 (2015).

    Article  CAS  PubMed  Google Scholar 

  17. Cardon, M., Loot, G., Grenouillet, G. & Blanchet, S. Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis. J. Anim. Ecol. 80, 657–667 (2011).

    Article  PubMed  Google Scholar 

  18. Mahmud, M. A., Bradley, J. E. & MacColl, A. D. C. Abiotic environmental variation drives virulence evolution in a fish host–parasite geographic mosaic. Funct. Ecol. 31, 2138–2146 (2017).

    Article  Google Scholar 

  19. Arruda, J. A., Marzolf, G. R. & Faulk, R. T. The role of suspended sediments in the nutrition of zooplankton in turbid reservoirs. Ecology 64, 1225–1235 (1983).

    Article  Google Scholar 

  20. Mostowy, R. & Engelstädter, J. The impact of environmental change on host–parasite coevolutionary dynamics. Proc. R. Soc. B 278, 2283–2292 (2011).

    Article  PubMed  Google Scholar 

  21. Thompson, J. N. The Geographic Mosaic of Coevolution (Univ. Chicago Press, 2005).

  22. Brett, M. T. Chaoborus and fish-mediated influences on Daphnia longispina population structure, dynamics and life history strategies. Oecologia 89, 69–77 (1992).

    Article  PubMed  Google Scholar 

  23. Goss, L. B. & Bunting, D. L. Daphnia development and reproduction: responses to temperature. J. Therm. Biol. 8, 375–380 (1983).

    Article  Google Scholar 

  24. Luijckx, P., Fienberg, H., Duneau, D. & Ebert, D. A matching-allele model explains host resistance to parasites. Curr. Biol. 23, 1085–1088 (2013).

    Article  CAS  PubMed  Google Scholar 

  25. Bento, G. et al. The genetic basis of resistance and matching-allele interactions of a host–parasite system: the Daphnia magna–Pasteuria ramosa model. PLoS Genet. 13, e1006596 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  26. Grosberg, R. K. Mate selection and the evolution of highly polymorphic self/nonself recognition genes. Science 289, 2111–2114 (2000).

    Article  CAS  PubMed  Google Scholar 

  27. Hutchinson, G. E. The Ecological Theater and the Evolutionary Play (Yale Univ. Press, 1965).

  28. Stuart, Y. E. et al. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat. Ecol. Evol. 1, 0158 (2017).

    Article  Google Scholar 

  29. Klüttgen, B., Dülmer, U., Engels, M. & Ratte, H. ADaM, an artificial freshwater for the culture of zooplankton. Water Res. 28, 743–746 (1994).

    Article  Google Scholar 

  30. Ebert, D., Zschokke-Rohringer, C. D. & Carius, H. J. Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa. Proc. R. Soc. B 265, 2127–2134 (1998).

    Article  PubMed Central  Google Scholar 

  31. Auld, S. K. J. R. & Brand, J. Simulated climate change, epidemic size, and host evolution across host–parasite populations. Glob. Change Biol. 23, 5045–5053 (2017).

    Article  Google Scholar 

  32. Holm, S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65–70 (1979).

    Google Scholar 

  33. R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  34. Brereton, R. G. & Lloyd, G. R. Re-evaluating the role of the Mahalanobis distance measure. J. Chemom. 30, 134–143 (2016).

    Article  CAS  Google Scholar 

  35. D’Orazio, M. StatMatch: Statistical Matching or Data Fusion. R package version 1.4.0 (2019).

  36. Goslee, S. C. & Urban, D. L. The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 22, 1–22 (2007).

    Article  Google Scholar 

  37. Lefcheck, J. S. piecewiseSEM: piecewise structural equation modelling in R for ecology, evolution and systematics. Methods Ecol. Evol. 7, 573–579 (2016).

    Article  Google Scholar 

  38. Auld, S. K. J. R., Wilson, P. J. & Little, T. J. Rapid change in parasite infection traits over the course of an epidemic in a wild host–parasite population. Oikos 123, 232–238 (2014).

    Article  Google Scholar 

  39. Shocket, M. S. et al. Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics. Ecology 99, 1975–1987 (2018).

    Article  PubMed  Google Scholar 

  40. Duncan, A. B., Mitchell, S. E. & Little, T. J. Parasite-mediated selection and the role of sex and diapause in Daphnia. J. Evol. Biol. 19, 1183–1189 (2006).

    Article  CAS  PubMed  Google Scholar 

  41. Auld, S. K. J. R. et al. Variation in costs of parasite resistance among natural host populations. J. Evol. Biol. 26, 2479–2486 (2013).

    Article  CAS  PubMed  Google Scholar 

  42. Laine, A.-L. Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales. Proc. R. Soc. B 273, 267–273 (2006).

    Article  PubMed  Google Scholar 

  43. Lohse, K., Gutierrez, A. & Kaltz, O. Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution 60, 1177–1186 (2006).

    PubMed  Google Scholar 

  44. Duffy, M. A. & Sivars-Becker, L. Rapid evolution and ecological host–parasite dynamics. Ecol. Lett. 10, 44–53 (2007).

    Article  PubMed  Google Scholar 

  45. Brewer, M. J., Butler, A. & Cooksley, S. L. The relative performance of AIC, AICC and BIC in the presence of unobserved heterogeneity. Methods Ecol. Evol. 7, 679–692 (2016).

    Article  Google Scholar 

  46. Shipley, B. A new inferential test for path models based on directed acyclic graphs. Struct. Equ. Model. 7, 206–218 (2000).

    Article  Google Scholar 

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Acknowledgements

We thank M. Tinsley, S. Thackeray and the Stirling Eco-Evo group for comments on this manuscript. This work was supported by NERC Independent Research Fellowship (NE/L011549/1) and Royal Society Research Grant (RG130657) to S.K.J.R.A.

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Authors and Affiliations

  1. Biological and Environmental Sciences, University of Stirling, Stirling, UK

    Sam Paplauskas, June Brand & Stuart K. J. R. Auld

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Contributions

Conceptualization: S.K.J.R.A.; data curation: S.K.J.R.A.; formal analysis: S.P. and S.K.J.R.A.; funding acquisition: S.K.J.R.A.; investigation: S.P., J.B. and S.K.J.R.A.; methodology: S.P., J.B. and S.K.J.R.A.; supervision: S.K.J.R.A.; writing original draft: S.P. and S.K.J.R.A.; writing, review and editing: all authors.

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Correspondence to Stuart K. J. R. Auld.

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Paplauskas, S., Brand, J. & Auld, S.K.J.R. Ecology directs host–parasite coevolutionary trajectories across Daphnia–microparasite populations. Nat Ecol Evol 5, 480–486 (2021). https://doi.org/10.1038/s41559-021-01390-7

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