Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids

  1. Lisa Horn  Is a corresponding author
  2. Thomas Bugnyar
  3. Michael Griesser
  4. Marietta Hengl
  5. Ei-Ichi Izawa
  6. Tim Oortwijn
  7. Christiane Rössler
  8. Clara Scheer
  9. Martina Schiestl
  10. Masaki Suyama
  11. Alex H Taylor
  12. Lisa-Claire Vanhooland
  13. Auguste M P von Bayern
  14. Yvonne Zürcher
  15. Jorg JM Massen
  1. University of Vienna, Austria
  2. University of Zurich, Switzerland
  3. Keio University, Japan
  4. Max Planck Institute for the Science of Human History, Germany
  5. Hokkaido University, Japan
  6. University of Auckland, New Zealand
  7. Max Planck Institute for Ornithology, Germany
  8. Zurich University, Switzerland
  9. Utrecht University, Netherlands

Abstract

The investigation of prosocial behavior is of particular interest from an evolutionary perspective. Comparisons of prosociality across non-human animal species have, however, so far largely focused on primates, and their interpretation is hampered by the diversity of paradigms and procedures used. Here we present the first systematic comparison of prosocial behavior across multiple species in a taxonomic group outside the primate order, namely the bird family Corvidae. We measured prosociality in 8 corvid species, which vary in the expression of cooperative breeding and colonial nesting. We show that cooperative breeding is positively associated with prosocial behavior across species. Also, colonial nesting is associated with a stronger propensity for prosocial behavior, but only in males. The combined results of our study strongly suggest that both cooperative breeding and colonial nesting, which may both rely on heightened social tolerance at the nest, are likely evolutionary pathways to prosocial behavior in corvids.

Data availability

The datasets analyzed in this study are available on Dryad.

The following data sets were generated

Article and author information

Author details

  1. Lisa Horn

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    For correspondence
    lisa.horn@univie.ac.at
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9586-915X
  2. Thomas Bugnyar

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael Griesser

    Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2220-2637
  4. Marietta Hengl

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  5. Ei-Ichi Izawa

    Department of Psychology, Keio University, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Tim Oortwijn

    Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  7. Christiane Rössler

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  8. Clara Scheer

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  9. Martina Schiestl

    Department of Linguistic and Cultural Evolution, Max Planck Institute for the Science of Human History, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Masaki Suyama

    Department of Behavioral Sciences, Hokkaido University, Sapporo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  11. Alex H Taylor

    School of Psychology, University of Auckland, Auckland, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  12. Lisa-Claire Vanhooland

    Department of Behavioral and Cognitive Biology, University of Vienna, Vienna, Austria
    Competing interests
    The authors declare that no competing interests exist.
  13. Auguste M P von Bayern

    Research Group Comparative Cognition, Max Planck Institute for Ornithology, Seewiesen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Yvonne Zürcher

    Department of Anthropology, Zurich University, Zurich, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
  15. Jorg JM Massen

    Animal Ecology Group, Department of Biology, Utrecht University, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.

Funding

Austrian Science Fund (P26806)

  • Jorg JM Massen

JST CREST (JPMJCR17A4)

  • Ei-Ichi Izawa

Keio University ICR Projects (MKJ1905)

  • Ei-Ichi Izawa

Royal Society of New Zealand (Rutherford Discovery Fellowship)

  • Alex H Taylor

Prime Minister's McDiarmid Emerging Scientist Prize

  • Alex H Taylor

University of Vienna (Marie Jahoda grant)

  • Lisa Horn

Austrian Science Fund (Y366-B17)

  • Thomas Bugnyar

Vienna Science and Technology Fund (CS11-008)

  • Thomas Bugnyar

ERA-Net BiodivERsA (31BD30_172465)

  • Michael Griesser

University of Vienna (Förderungsstipendium)

  • Marietta Hengl
  • Christiane Rössler

University of Vienna (Uni:Docs doctoral fellowship)

  • Lisa-Claire Vanhooland

JSPS KAKENHI (17H02653)

  • Ei-Ichi Izawa

JSPS KAKENHI (16H06324)

  • Ei-Ichi Izawa

JSPS KAKENHI (15J02148)

  • Masaki Suyama

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

Ethics

Animal experimentation: The study followed the Guidelines for the Use of Animals (81), in accordance with national legislations. All animal care and data collection protocols were reviewed and approved by the ethical boards of the respective research institutions (see SI, Table S7).

Copyright

© 2020, Horn 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

  • 2,767
    views
  • 311
    downloads
  • 25
    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. Lisa Horn
  2. Thomas Bugnyar
  3. Michael Griesser
  4. Marietta Hengl
  5. Ei-Ichi Izawa
  6. Tim Oortwijn
  7. Christiane Rössler
  8. Clara Scheer
  9. Martina Schiestl
  10. Masaki Suyama
  11. Alex H Taylor
  12. Lisa-Claire Vanhooland
  13. Auguste M P von Bayern
  14. Yvonne Zürcher
  15. Jorg JM Massen
(2020)
Sex-specific effects of cooperative breeding and colonial nesting on prosociality in corvids
eLife 9:e58139.
https://doi.org/10.7554/eLife.58139

Share this article

https://doi.org/10.7554/eLife.58139

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.