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An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts

Louise Solveig Nørgaard, View ORCID ProfileGiacomo Zilio, Camille Saade, Claire Gougat-Barbera, Matthew D. Hall, View ORCID ProfileEmanuel A. Fronhofer, Oliver Kaltz
doi: https://doi.org/10.1101/2020.01.31.928150
Louise Solveig Nørgaard
1School of Biological Sciences and Centre for Geometric Biology, Monash University, Melbourne 3800, Australia
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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  • For correspondence: oliver.kaltz@umontpellier.fr lnorga10@hotmail.com
Giacomo Zilio
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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  • ORCID record for Giacomo Zilio
Camille Saade
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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Claire Gougat-Barbera
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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Matthew D. Hall
1School of Biological Sciences and Centre for Geometric Biology, Monash University, Melbourne 3800, Australia
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Emanuel A. Fronhofer
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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  • ORCID record for Emanuel A. Fronhofer
Oliver Kaltz
2ISEM, University of Montpellier, CNRS, EPHE, IRD, Montpellier, France
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  • For correspondence: oliver.kaltz@umontpellier.fr lnorga10@hotmail.com
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ABSTRACT

Eco-evolutionary processes may play an important role in the spatial spread of infectious disease. Current theory predicts more exploitative parasites to evolve in highly connected populations or at the front of spreading epidemics. However, many parasites rely on host dispersal to reach new populations. This may lead to conflict between local transmission and global spread, possibly counteracting selection for higher virulence. Here, we used the freshwater host Paramecium caudatum and its bacterial parasite Holospora undulata to investigate parasite evolution under an experimental range expansion scenario with natural host dispersal. We find that parasites evolving at experimental range fronts favoured higher dispersal rates of infected hosts than did parasites evolving in core populations. Front parasites further showed lower levels of virulence (host division and survival) and delayed development of infection, consistent with parameter estimates from an epidemiological model that we fitted on experimental time-series data. This combined evidence suggests an evolutionary trade-off between virulence and host-mediated dispersal, with a concomitant reduction in the investment into horizontal transmission. Our experiment illustrates how parasite evolution can be shaped by divergent selection encountered in different segments of an epidemic wave. Such an interplay between demography and spatial selection has important implications for the understanding and management of emerging diseases, and, more generally, for biological invasions and other non-equilibrium scenarios of spreading populations.

SIGNIFICANCE STATEMENT What drives parasite evolution in spatially expanding epidemics? Many parasites require dispersal of infected hosts to reach new patches, and this may produce specific adaptations enhancing spatial spread. We performed experimental range expansions in an aquatic model system, with natural dispersal of infected hosts. Parasites from experimental range fronts were less virulent and interfered less with host dispersal, but also invested less in horizontal transmission than parasites from the range core. Thus, dispersal adaptation at the front may come at a cost of reduced horizontal transmission, a trade-off rarely considered in theoretical models on parasite virulence evolution. These results have important implications in the context of emerging diseases, and for parasite evolution during biological invasions or other spatial non-equilibrium scenarios.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Shared first author contribution

  • Analysis and discussion clarified, Figures updated; Supplementary section updated

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC 4.0 International license.
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Posted July 11, 2020.
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An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts
Louise Solveig Nørgaard, Giacomo Zilio, Camille Saade, Claire Gougat-Barbera, Matthew D. Hall, Emanuel A. Fronhofer, Oliver Kaltz
bioRxiv 2020.01.31.928150; doi: https://doi.org/10.1101/2020.01.31.928150
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An evolutionary trade-off between parasite virulence and dispersal at experimental invasion fronts
Louise Solveig Nørgaard, Giacomo Zilio, Camille Saade, Claire Gougat-Barbera, Matthew D. Hall, Emanuel A. Fronhofer, Oliver Kaltz
bioRxiv 2020.01.31.928150; doi: https://doi.org/10.1101/2020.01.31.928150

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