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Hunting alters viral transmission and evolution in a large carnivore

Nature Ecology & Evolution volume 6, pages 174–182 (2022)Cite this article

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Abstract

Hunting can fundamentally alter wildlife population dynamics but the consequences of hunting on pathogen transmission and evolution remain poorly understood. Here, we present a study that leverages a unique landscape-scale quasi-experiment coupled with pathogen-transmission tracing, network simulation and phylodynamics to provide insights into how hunting shapes feline immunodeficiency virus (FIV) dynamics in puma (Puma concolor). We show that removing hunting pressure enhances the role of males in transmission, increases the viral population growth rate and increases the role of evolutionary forces on the pathogen compared to when hunting was reinstated. Changes in transmission observed with the removal of hunting could be linked to short-term social changes while the male puma population increased. These findings are supported through comparison with a region with stable hunting management over the same time period. This study shows that routine wildlife management can have impacts on pathogen transmission and evolution not previously considered.

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Fig. 1: The transmission of FIVpco was dominated by males in the treatment region, whereas females were more central in the stable management region.
Fig. 2: Predicted FIVpco transmission events and their estimated timing among puma involved in a transmission chain.
Fig. 3: The elimination of puma hunting in the treatment region led to an increase in FIVpco diversity that correlated positively with male population size.

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Data availability

DNA sequences are GenBank accessions MN563193–MN563239. All other data and code to perform the analysis are available on Github at https://github.com/nfj1380/Transmission-dynamics_huntingPumaFIV65

Code availability

The code and data to perform these operations as well as the transmission tree analysis above can be found here: https://github.com/nfj1380/Transmission-dynamics_huntingPumaFIV65

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Acknowledgements

This project was funded by the National Science Foundation Ecology of Infectious Diseases research programme grants (DEB 1413925) (S.V., W.C.F., M.E.C., K.C. and S.C.) and an Australian Research Council Discovery Project Grant (DP190102020) (M.C., S.C., M.E.C. and S.V.). M.L.J.G. was supported by the Office of the Director, National Institutes of Health (NIH) under award no. NIH T32OD010993. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. S.D. is supported by the Fonds National de la Recherche Scientifique (FNRS, Belgium). G.B. acknowledges support from the Interne Fondsen KU Leuven/Internal Funds KU Leuven under grant agreement C14/18/094 and the Research Foundation—Flanders (‘Fonds voor Wetenschappelijk Onderzoek—Vlaanderen’, G0E1420N). M.E.C. was funded by the National Science Foundation (DEB 1654609 and 2030509) and the College of Veterinary Medicine Research Office UMN Ag Experiment Station General Ag Research Funds. X.D. was supported by the National Institute for Health Research Health Protection Research Unit in Genomics and Enabling Data. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the US Government.

Author information

Authors and Affiliations

  1. Department of Veterinary Population Medicine, University of Minnesota, St Paul, MN, USA

    Nicholas M. Fountain-Jones, Marie L. J. Gilbertson & Meggan E. Craft

  2. School of Natural Sciences, University of Tasmania, Hobart, Tasmania, Australia

    Nicholas M. Fountain-Jones, Michael Charleston & Scott Carver

  3. Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO, USA

    Simona Kraberger, Roderick B. Gagne & Sue VandeWoude

  4. Department of Biology, Colorado State University, Fort Collins, CO, USA

    Daryl R. Trumbo, Patricia E. Salerno & W. Chris Funk

  5. Centro de Investigación de la Biodiversidad y Cambio Climático (BioCamb), Facultad de Ciencias de Medio Ambiente, Universidad Tecnológica Indoamérica, Quito, Ecuador

    Patricia E. Salerno

  6. Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, USA

    W. Chris Funk

  7. Department of Fish, Wildlife, and Conservation Biology, Colorado State University, Fort Collins, CO, USA

    Kevin Crooks

  8. Colorado Parks and Wildlife, Montrose, CO, USA

    Kenneth Logan

  9. Colorado Parks and Wildlife, Fort Collins, CO, USA

    Mathew Alldredge

  10. Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Brussels, Belgium

    Simon Dellicour

  11. Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, Leuven, Belgium

    Simon Dellicour & Guy Baele

  12. School of Life Sciences and Department of Statistics, University of Warwick, Coventry, UK

    Xavier Didelot

  13. Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, MN, USA

    Meggan E. Craft

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  1. Nicholas M. Fountain-Jones
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Contributions

N.M.F.J. conducted the analysis and wrote the initial draft of the paper to which all authors contributed. K.L. and M.A. studied the puma populations in the field and provided the blood samples. S.K., D.R.T., P.S., R.G. and S.V. collected virus and host genetic data. S.D., G.B., M.C. and X.D. contributed to the phylogenetic and transmission tree analyses. M.L.J.G. contributed to the spatial analysis. M.E.C., S.V., K.C., W.C.F. and S.C. conceived of the project.

Corresponding author

Correspondence to Nicholas M. Fountain-Jones.

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Competing interests

The authors declare no competing interests.

Animal care statement

Puma samples were collected as part of ongoing studies by CPW between 2006 and 2014. We handled all pumas in accordance with approved CPW ACUC capture and handling protocols (ACUC file no. 08-2004, ACUC protocol nos. 03-2007 and 16‐2008). Samples were provided to Colorado State University for diagnostic evaluation. Colorado State University and CPW Institutional Animal Care and Use Committees reviewed and approved this work before initiation (CSU IACUC protocol 05-061A).

Peer review information

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

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

Extended data

Extended Data Fig. 1 Probabilities of transmission between pairs of individuals in both regions.

The left panel (a) shows the treatment region and the right panel (b) shows the stable region.

Extended Data Fig. 2 Realized generation time distributions (time from infection to onward transmission) by region.

The top panel (a) shows the treatment region and the bottom panel (b) shows the stable region. In both regions, onward transmission events for FIVpco were most likely in the first two years after infection.

Extended Data Fig. 3 Estimated number of unsampled vs. sampled cases by region.

The top panel (a) shows the treatment region and the bottom panel (b) shows the stable region.

Extended Data Fig. 4 Histograms showing the expected homophily weighted degree distribution from our simulated networks by region (that is, just including edges from males-males) compared to observed homophily weight degree values.

The left panel (a) shows the treatment region and the right panel (b) shows the stable region. (see Methods -simulation modelling for details).

Extended Data Fig. 5 Time distributions for individuals involved in a putative transmission chain with the likely direction (red arrows) and the spatial context on each transmission event.

See Fig. 2 for other putative transmission events in the treatment region. Light yellow background: hunting pressure relieved, red background: hunting pressure resumed. White arrows in the maps indicate the likely transmission direction. Birth, death and sampling date is provided under each silhouette and estimated birth year is indicated by the black arrow. Colour of the boxes reflects transmission chain identity. M114 and F136 had overlapping home ranges and potentially transmitted FIVpco during mating event(s). M55 and F94 also had overlapping home ranges, and M55 was likely the sire of F94’s kittens; the pair consorted on 15 April 2010 and kittens were born on 15 July 2010. In addition, M55 associated with this family when the kittens were nurslings (K. Logan observation). Maps Data: Google ©2020.

Extended Data Fig. 6 Infection time distributions in the stable region for individuals involved in a putative transmission chain with the likely direction (red arrows) and the spatial context on each transmission event.

Colour of the boxes reflects transmission chain identity and grey boxes indicates sampling period. Sex, sampling date, birth date and death date of each individual are provided in each box when known. Maps Data: Google ©2020.

Extended Data Fig. 7 Map of our study regions.

Top panel: the location of all individuals sampled in 2005–2009 (no hunting in the treatment region). Bottom panel: the location of all individuals sampled (2005–2014 including the years when hunting was resumed in the treatment region). White diagonal lines show the broad extent of the Denver metropolitan area. Maps Data: Google ©2020.

Extended Data Fig. 8 Skyline plots showing the effective population size through time of dominant FIVpco lineages in each region.

The top panel (a) shows the treatment region and the bottom panel (b) shows the stable region. Grey shading provides the 95% high posterior density (HPD) estimates. a) Light yellow: hunting pressure relieved, red: hunting period, grey background: stable region. c) skygrowth plot from the management stable region showing FIVpco growth rate through time (see Fig. 3b in the main text for the corresponding plot from the treatment region). The dashed horizontal line reflects the 0-growth line.

Extended Data Fig. 9 FIVpco prevalence through time for each region. The top panel (a) shows the treatment region and the bottom panel (b) shows the stable region.

Numbers next to the points indicate how many samples were screened using qPCR each year. Confidence intervals were calculated using a binomial distribution and are only shown for total population estimates rather than for each sex (to aid interpretation). a) Light yellow: hunting pressure relieved, red: hunting period.

Extended Data Fig. 10 There were only insignificant relationships between FIVpco prevalence, growth rate and population size estimates.

(a) FIVpco growth rate (b) estimated puma population size, (c) female and (d) male population sizes in the treatment region. All data are scaled. Similar data was not available for the stable region. R: R2.

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Fountain-Jones, N.M., Kraberger, S., Gagne, R.B. et al. Hunting alters viral transmission and evolution in a large carnivore. Nat Ecol Evol 6, 174–182 (2022). https://doi.org/10.1038/s41559-021-01635-5

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