Cross-species transmission and evolutionary dynamics of canine distemper virus during a spillover in African lions of Serengeti National Park

Julie K. Weckworth, Brian W. Davis, Edward Dubovi, Nicholas Fountain-Jones, Craig Packer, Sarah Cleaveland, Meggan E. Craft, Ernest Eblate, Michael Schwartz, L. Scott Mills, Melody Roelke-Parker

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

The outcome of pathogen spillover from a reservoir to a novel host population can range from a “dead-end” when there is no onward transmission in the recipient population, to epidemic spread and even establishment in new hosts. Understanding the evolutionary epidemiology of spillover events leading to discrete outcomes in novel hosts is key to predicting risk and can lead to a better understanding of the mechanisms of emergence. Here we use a Bayesian phylodynamic approach to examine cross-species transmission and evolutionary dynamics during a canine distemper virus (CDV) spillover event causing clinical disease and population decline in an African lion population (Panthera leo) in the Serengeti Ecological Region between 1993 and 1994. Using 21 near-complete viral genomes from four species we found that this large-scale outbreak was likely ignited by a single cross-species spillover event from a canid reservoir to noncanid hosts <1 year before disease detection and explosive spread of CDV in lions. Cross-species transmission from other noncanid species probably fuelled the high prevalence of CDV across spatially structured lion prides. Multiple lines of evidence suggest that spotted hyenas (Crocuta crocuta) could have acted as the proximate source of CDV exposure in lions. We report 13 nucleotide substitutions segregating CDV strains found in canids and noncanids. Our results are consistent with the hypothesis that virus evolution played a role in CDV emergence in noncanid hosts following spillover during the outbreak, suggest that host barriers to clinical infection can limit outcomes of CDV spillover in novel host species.

Original languageEnglish (US)
Pages (from-to)4308-4321
Number of pages14
JournalMolecular ecology
Volume29
Issue number22
DOIs
StatePublished - Nov 1 2020

Bibliographical note

Funding Information:
We thank Linda Munson for critical contributions made in documenting and diagnosing CDV as the cause of the 1993?1994 epidemic. The Messerli Foundation in Zurich, Switzerland, provided funding for sample collection and field research. We are grateful to Tamara Max, Amy Glaser, Melissa Laverack, Nancy Cavender Zylich and Christian Leutenegger for providing technical assistance, and Vanessa Ezenwa, Gordon Luikart, Angie Luis, Mark Hebblewhite, Hugh Robinson, Byron Weckworth and Gretchen Grimes for helpful comments on study design and/or earlier drafts of the manuscript. Funding for this study was provided by the Morris Animal Foundation, grant ID D14ZO-013, ?Understanding spillover of a deadly virus in a well-studied African lion population.? This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant #DGE-0809127 and the National Science Foundation grant #DGE-0504628.

Funding Information:
We thank Linda Munson for critical contributions made in documenting and diagnosing CDV as the cause of the 1993–1994 epidemic. The Messerli Foundation in Zurich, Switzerland, provided funding for sample collection and field research. We are grateful to Tamara Max, Amy Glaser, Melissa Laverack, Nancy Cavender Zylich and Christian Leutenegger for providing technical assistance, and Vanessa Ezenwa, Gordon Luikart, Angie Luis, Mark Hebblewhite, Hugh Robinson, Byron Weckworth and Gretchen Grimes for helpful comments on study design and/or earlier drafts of the manuscript. Funding for this study was provided by the Morris Animal Foundation, grant ID D14ZO‐013, “Understanding spillover of a deadly virus in a well‐studied African lion population.” This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant #DGE‐0809127 and the National Science Foundation grant #DGE‐0504628.

Publisher Copyright:
© 2020 John Wiley & Sons Ltd

Keywords

  • African lion
  • Serengeti
  • canine distemper virus
  • carnivore conservation
  • evolutionary epidemiology
  • pathogen spillover

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