Wide-ranging consequences of priority effects governed by an overarching factor

  1. Callie Rodgers Chappell  Is a corresponding author
  2. Manpreet K Dhami
  3. Mark C Bitter
  4. Lucas Czech
  5. Sur Herrera Paredes
  6. Fatoumata Binta Barrie
  7. Yadira Calderón
  8. Katherine Eritano
  9. Lexi-Ann Golden
  10. Daria Hekmat-Scafe
  11. Veronica Hsu
  12. Clara Kieschnick
  13. Shyamala Malladi
  14. Nicole Rush
  15. Tadashi Fukami  Is a corresponding author
  1. Stanford University, United States
  2. Manaaki Whenua - Landcare Research, New Zealand
  3. Carnegie Institution for Science, United States
  4. University of California, Santa Barbara, United States

Abstract

Priority effects, where arrival order and initial relative abundance modulate local species interactions, can exert taxonomic, functional, and evolutionary influences on ecological communities by driving them to alternative states. It remains unclear if these wide-ranging consequences of priority effects can be explained systematically by a common underlying factor. Here, we identify such a factor in an empirical system. In a series of field and laboratory studies, we focus on how pH affects nectar-colonizing microbes and their interactions with plants and pollinators. In a field survey, we found that nectar microbial communities in a hummingbird-pollinated shrub, Diplacus (formerly Mimulus) aurantiacus, exhibited abundance patterns indicative of alternative stable states that emerge through domination by either bacteria or yeasts within individual flowers. In addition, nectar pH varied among D. aurantiacus flowers in a manner that is consistent with the existence of these alternative stable states. In laboratory experiments, Acinetobacter nectaris, the bacterium most commonly found in D. aurantiacus nectar, exerted a strongly negative priority effect against Metschnikowia reukaufii, the most common nectar-specialist yeast, by reducing nectar pH. This priority effect likely explains the mutually exclusive pattern of dominance found in the field survey. Furthermore, experimental evolution simulating hummingbird-assisted dispersal between flowers revealed that M. reukaufii could evolve rapidly to improve resistance against the priority effect if constantly exposed to A. nectaris-induced pH reduction. Finally, in a field experiment, we found that low nectar pH could reduce nectar consumption by hummingbirds, suggesting functional consequences of the pH-driven priority effect for plant reproduction. Taken together, these results show that it is possible to identify an overarching factor that governs the eco-evolutionary dynamics of priority effects across multiple levels of biological organization.

Data availability

Raw sequencing reads are available at NCBI Sequence Read Archive (BioProject PRJNA825574). All other data and code reported in this paper are available at: https://gitlab.com/teamnectarmicrobe/n06_nectarmicrobes_ecoevo

The following data sets were generated

Article and author information

Author details

  1. Callie Rodgers Chappell

    Department of Biology, Stanford University, Stanford, United States
    For correspondence
    calliech@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4611-0021
  2. Manpreet K Dhami

    Biocontrol and Molecular Ecology, Manaaki Whenua - Landcare Research, Lincoln, New Zealand
    Competing interests
    The authors declare that no competing interests exist.
  3. Mark C Bitter

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7607-2375
  4. Lucas Czech

    Department of Plant Biology, Carnegie Institution for Science, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1340-9644
  5. Sur Herrera Paredes

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Fatoumata Binta Barrie

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Yadira Calderón

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Katherine Eritano

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Lexi-Ann Golden

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Daria Hekmat-Scafe

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Veronica Hsu

    Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Goleta, United States
    Competing interests
    The authors declare that no competing interests exist.
  12. Clara Kieschnick

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Shyamala Malladi

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Nicole Rush

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  15. Tadashi Fukami

    Department of Biology, Stanford University, Stanford, United States
    For correspondence
    fukamit@stanford.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5654-4785

Funding

National Science Foundation (DEB 1149600)

  • Tadashi Fukami

National Science Foundation (DEB 1737758)

  • Tadashi Fukami

National Science Foundation (DGE 1656518)

  • Callie Rodgers Chappell

Marsden Fund (MFP-LCR-2002)

  • Manpreet K Dhami

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

Reviewing Editor

  1. Maureen L Coleman, University of Chicago, United States

Version history

  1. Preprint posted: April 20, 2022 (view preprint)
  2. Received: April 21, 2022
  3. Accepted: October 26, 2022
  4. Accepted Manuscript published: October 27, 2022 (version 1)
  5. Version of Record published: November 17, 2022 (version 2)

Copyright

© 2022, Chappell 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.

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  1. Callie Rodgers Chappell
  2. Manpreet K Dhami
  3. Mark C Bitter
  4. Lucas Czech
  5. Sur Herrera Paredes
  6. Fatoumata Binta Barrie
  7. Yadira Calderón
  8. Katherine Eritano
  9. Lexi-Ann Golden
  10. Daria Hekmat-Scafe
  11. Veronica Hsu
  12. Clara Kieschnick
  13. Shyamala Malladi
  14. Nicole Rush
  15. Tadashi Fukami
(2022)
Wide-ranging consequences of priority effects governed by an overarching factor
eLife 11:e79647.
https://doi.org/10.7554/eLife.79647

Share this article

https://doi.org/10.7554/eLife.79647

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