Ecological multiplex interactions determine the role of species for parasite spread amplification

  1. Massimo Stella
  2. Sanja Selakovic
  3. Alberto Antonioni
  4. Cecilia Andreazzi  Is a corresponding author
  1. University of Southampton, United Kingdom
  2. Utrecht University, Netherlands
  3. University College London, United Kingdom
  4. Fundação Oswaldo Cruz, Brazil

Abstract

Despite their potential interplay, multiple routes of many disease transmissions are often investigated separately. As an unifying framework for understanding parasite spread through interdependent transmission paths, we present the 'ecomultiplex' model, where the multiple transmission paths among a diverse community of interacting hosts are represented as a spatially explicit multiplex network. We adopt this framework for designing and testing potential control strategies for T. cruzi spread in two empirical host communities. We show that the ecomultiplex model is an efficient and low data-demanding method to identify which species enhances parasite spread and should thus be a target for control strategies. We also find that the interplay between predator-prey and host-parasite interactions leads to a phenomenon of parasite amplification, in which top predators facilitate T. cruzi spread, offering a mechanistic interpretation of previous empirical findings. Our approach can provide novel insights in understanding and controlling parasite spreading in real-world complex systems.

Data availability

All data generated or analysed during this study are included in the manuscript and appendices.

Article and author information

Author details

  1. Massimo Stella

    Institute for Complex Systems Simulation, University of Southampton, Southampton, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Sanja Selakovic

    Faculty of Geociences, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Alberto Antonioni

    Department of Economics, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Cecilia Andreazzi

    Fiocruz Mata Atlântica, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil
    For correspondence
    cecilia.andreazzi@fiocruz.br
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9817-0635

Funding

Swiss National Science Foundation (P2LAP1-161864)

  • Alberto Antonioni

Netherlands Organization for Scientific Research (645.000.013)

  • Sanja Selakovic

Engineer Research and Development Center (EP/G03690X/1)

  • Massimo Stella

Netherlands Organization for Scientific Research (647570)

  • Sanja Selakovic

Swiss National Science Foundation (P300P1-171537)

  • Alberto Antonioni

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2018, Stella et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,533
    views
  • 247
    downloads
  • 11
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Massimo Stella
  2. Sanja Selakovic
  3. Alberto Antonioni
  4. Cecilia Andreazzi
(2018)
Ecological multiplex interactions determine the role of species for parasite spread amplification
eLife 7:e32814.
https://doi.org/10.7554/eLife.32814

Share this article

https://doi.org/10.7554/eLife.32814

Further reading

    1. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.

    1. Ecology
    2. Neuroscience
    Kathleen T Quach, Gillian A Hughes, Sreekanth H Chalasani
    Research Article

    Prey must balance predator avoidance with feeding, a central dilemma in prey refuge theory. Additionally, prey must assess predatory imminence—how close threats are in space and time. Predatory imminence theory classifies defensive behaviors into three defense modes: pre-encounter, post-encounter, and circa-strike, corresponding to increasing levels of threat—–suspecting, detecting, and contacting a predator. Although predatory risk often varies in spatial distribution and imminence, how these factors intersect to influence defensive behaviors is poorly understood. Integrating these factors into a naturalistic environment enables comprehensive analysis of multiple defense modes in consistent conditions. Here, we combine prey refuge and predatory imminence theories to develop a model system of nematode defensive behaviors, with Caenorhabditis elegans as prey and Pristionchus pacificus as predator. In a foraging environment comprised of a food-rich, high-risk patch and a food-poor, low-risk refuge, C. elegans innately exhibits circa-strike behaviors. With experience, it learns post- and pre-encounter behaviors that proactively anticipate threats. These defense modes intensify with predator lethality, with only life-threatening predators capable of eliciting all three modes. SEB-3 receptors and NLP-49 peptides, key stress regulators, vary in their impact and interdependence across defense modes. Overall, our model system reveals fine-grained insights into how stress-related signaling regulates defensive behaviors.