Antagonistic Effects of Intraspecific Cooperation and Interspecific Competition on Thermal Performance

  1. Hsiang-Yu Tsai
  2. Dustin Reid Rubenstein
  3. Bo-Fei Chen
  4. Mark Liu
  5. Shih-Fan Chan
  6. De-Pei Chen
  7. Syuan-Jyun Sun
  8. Tzu-Neng Yuan
  9. Sheng-Feng Shen  Is a corresponding author
  1. Biodiversity Research Center, Academia Sinica, Taiwan, Republic of China
  2. Columbia University, United States
  3. Biodiversity Research Center, Academia Sinica, Taiwan

Abstract

Understanding how climate-mediated biotic interactions shape thermal niche width is critical in an era of global change. Yet, most previous work on thermal niches has ignored detailed mechanistic information about the relationship between temperature and organismal performance, which can be described by a thermal performance curve. Here, we develop a model that predicts the width of thermal performance curves will be narrower in the presence of interspecific competitors, causing a species' optimal breeding temperature to diverge from that of its competitor. We test this prediction in the Asian burying beetle Nicrophorus nepalensis, confirming that the divergence in actual and optimal breeding temperatures is the result of competition with their primary competitor, blowflies. However, we further show that intraspecific cooperation enables beetles to outcompete blowflies by recovering their optimal breeding temperature. Ultimately, linking abiotic factors and biotic interactions on niche width will be critical for understanding species-specific responses to climate change.

Data availability

All data analysed during the study are available in Dryad.

The following data sets were generated
    1. Shen
    2. Sheng-Feng et al
    (2020) Source data for empirical experiments
    Dryad Digital Repository, doi.org/10.5061/dryad.w0vt4b8nw.

Article and author information

Author details

  1. Hsiang-Yu Tsai

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  2. Dustin Reid Rubenstein

    Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bo-Fei Chen

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3005-8724
  4. Mark Liu

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  5. Shih-Fan Chan

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  6. De-Pei Chen

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  7. Syuan-Jyun Sun

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  8. Tzu-Neng Yuan

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    Competing interests
    The authors declare that no competing interests exist.
  9. Sheng-Feng Shen

    Biodiversity Research Center, Biodiversity Research Center, Academia Sinica, Taipei, Taiwan, Republic of China
    For correspondence
    shensf@sinica.edu.tw
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0631-6343

Funding

Ministry of Science and Technology, Taiwan (103-2621-B-001 -003 -MY3)

  • Sheng-Feng Shen

National Science Foundation (IOS-1656098)

  • Dustin Reid Rubenstein

Ministry of Science and Technology, Taiwan (101-2313-B-001 -008 -MY3)

  • Sheng-Feng Shen

Academia Sinica (AS-SS-106-05)

  • Sheng-Feng Shen

Academia Sinica (AS-IA-106-L01)

  • Sheng-Feng Shen

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

Reviewing Editor

  1. Samuel L Díaz-Muñoz, University of California, Davis, United States

Publication history

  1. Received: March 18, 2020
  2. Accepted: July 28, 2020
  3. Accepted Manuscript published: August 18, 2020 (version 1)
  4. Version of Record published: August 21, 2020 (version 2)

Copyright

© 2020, Tsai 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

  • 1,701
    Page views
  • 166
    Downloads
  • 3
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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. Hsiang-Yu Tsai
  2. Dustin Reid Rubenstein
  3. Bo-Fei Chen
  4. Mark Liu
  5. Shih-Fan Chan
  6. De-Pei Chen
  7. Syuan-Jyun Sun
  8. Tzu-Neng Yuan
  9. Sheng-Feng Shen
(2020)
Antagonistic Effects of Intraspecific Cooperation and Interspecific Competition on Thermal Performance
eLife 9:e57022.
https://doi.org/10.7554/eLife.57022

Further reading

    1. Ecology
    2. Epidemiology and Global Health
    Carolina Oliveira de Santana, Pieter Spealman, Gabriel G Perron
    Insight

    The global spread of antibiotic resistance could be due to a number of factors, and not just the overuse of antibiotics in agriculture and medicine as previously thought.

    1. Ecology
    2. Evolutionary Biology
    Naïma Madi, Daisy Chen ... Nandita R Garud
    Research Advance Updated

    How the ecological process of community assembly interacts with intra-species diversity and evolutionary change is a longstanding question. Two contrasting hypotheses have been proposed: Diversity Begets Diversity (DBD), in which taxa tend to become more diverse in already diverse communities, and Ecological Controls (EC), in which higher community diversity impedes diversification. Previously, using 16S rRNA gene amplicon data across a range of microbiomes, we showed a generally positive relationship between taxa diversity and community diversity at higher taxonomic levels, consistent with the predictions of DBD (Madi et al., 2020). However, this positive 'diversity slope' plateaus at high levels of community diversity. Here we show that this general pattern holds at much finer genetic resolution, by analyzing intra-species strain and nucleotide variation in static and temporally sampled metagenomes from the human gut microbiome. Consistent with DBD, both intra-species polymorphism and strain number were positively correlated with community Shannon diversity. Shannon diversity is also predictive of increases in polymorphism over time scales up to ~4-6 months, after which the diversity slope flattens and becomes negative – consistent with DBD eventually giving way to EC. Finally, we show that higher community diversity predicts gene loss at a future time point. This observation is broadly consistent with the Black Queen Hypothesis, which posits that genes with functions provided by the community are less likely to be retained in a focal species' genome. Together, our results show that a mixture of DBD, EC, and Black Queen may operate simultaneously in the human gut microbiome, adding to a growing body of evidence that these eco-evolutionary processes are key drivers of biodiversity and ecosystem function.