Vector population growth and condition-dependent movement drive the spread of plant pathogens

Allison K. Shaw, Angela Peace, Alison G. Power, Nilsa A. Bosque-Pérez

Research output: Contribution to journalArticlepeer-review

23 Scopus citations

Abstract

Plant viruses, often spread by arthropod vectors, impact natural and agricultural ecosystems worldwide. Intuitively, the movement behavior and life history of vectors influence pathogen spread, but the relative contribution of each factor has not been examined. Recent research has highlighted the influence of host infection status on vector behavior and life history. Here, we developed a model to explore how vector traits influence the spread of vector-borne plant viruses. We allowed vector life history (growth rate, carrying capacity) and movement behavior (departure and settlement rates) parameters to be conditional on whether the plant host is infected or healthy and whether the vector is viruliferous (carrying the virus) or not. We ran simulations under a wide range of parameter combinations and quantified the fraction of hosts infected over time. We also ran case studies of the model for Barley yellow dwarf virus, a persistently transmitted virus, and for Potato virus Y, a non-persistently transmitted virus. We quantified the relative importance of each parameter on pathogen spread using Latin hypercube sampling with the statistical partial rank correlation coefficient technique. We found two general types of mechanisms in our model that increased the rate of pathogen spread. First, increasing factors such as vector intrinsic growth rate, carrying capacity, and departure rate from hosts (independent of whether these factors were condition-dependent) led to more vectors moving between hosts, which increased pathogen spread. Second, changing condition-dependent factors such as a vector's preference for settling on a host with a different infection status than itself, and vector tendency to leave a host of the same infection status, led to increased contact between hosts and vectors with different infection statuses, which also increased pathogen spread. Overall, our findings suggest that vector population growth rates had the greatest influence on rates of virus spread, but rates of vector dispersal from infected hosts and from hosts of the same infection status were also very important. Our model highlights the importance of simultaneously considering vector life history and behavior to better understand pathogen spread. Although developed for plant viruses, our model could readily be utilized with other vector-borne pathogen systems.

Original languageEnglish (US)
Pages (from-to)2145-2157
Number of pages13
JournalEcology
Volume98
Issue number8
DOIs
StatePublished - Aug 2017

Bibliographical note

Funding Information:
We thank M. Igoe and two reviewers for feedback on previous manuscript versions. This work was conducted as a part of the Vector Movement and Disease Working Group at the National Institute for Mathematical and Biological Synthesis, sponsored by the National Science Foundation through NSF Award DBI-1300426, with additional support from The University of Tennessee, Knoxville. This material is based in part upon work supported by NSF IOS-1556674 to A. K. Shaw and NSF DEB-1015903 and USDA NIFA 2013-67013-21235 to A. G. Power.

Keywords

  • Barley yellow dwarf virus
  • Potato virus Y
  • condition dependence
  • disease epidemiology
  • movement ecology
  • vector movement
  • vector preference

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