Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity

  1. Guilhem Doulcier  Is a corresponding author
  2. Amaury Lambert
  3. Silvia De Monte
  4. Paul B Rainey
  1. École supérieure de physique et de chimie industrielle de la ville de Paris, PSL University, France
  2. Collège de France, France
  3. École Normale Supérieure, France
  4. Max Planck Institute for Evolutionary Biology, Germany

Abstract

Interactions among microbial cells can generate new chemistries and functions, but exploitation requires establishment of communities that reliably recapitulate community-level phenotypes. Using mechanistic mathematical models, we show how simple manipulations to population structure can exogenously impose Darwinian-like properties on communities. Such scaffolding causes communities to participate directly in the process of evolution by natural selection and drives the evolution of cell-level interactions to the point where, despite underlying stochasticity, derived communities give rise to offspring communities that faithfully re-establish parental phenotype. The mechanism is akin to a developmental process (developmental correction) that arises from density dependent interactions among cells. Knowledge of ecological factors affecting evolution of developmental correction has implications for understanding the evolutionary origin of major egalitarian transitions, symbioses, and for top-down engineering of microbial communities.

Data availability

The source code for all simulations and figures in the manuscript isavailable as a zip file uploaded with the manuscript and in a public gitrepository (https://gitlab.com/ecoevomath/estaudel).

Article and author information

Author details

  1. Guilhem Doulcier

    Laboratoire de Génétique de l'Evolution, CNRS UMR 8231, École supérieure de physique et de chimie industrielle de la ville de Paris, PSL University, Paris, France
    For correspondence
    guilhem.doulcier@ens.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3720-9089
  2. Amaury Lambert

    Center for Interdisciplinary Research in Biology(CIRB), Collège de France, Paris, France
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7248-9955
  3. Silvia De Monte

    Institut de Biologie de l'´Ecole Normale Sup´erieure, École Normale Supérieure, Paris, France
    Competing interests
    No competing interests declared.
  4. Paul B Rainey

    Department of Microbial Population Biology, Max Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    Paul B Rainey, PBR is a founder of MilliDrop InstrumentsReviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0879-5795

Funding

Agence Nationale de la Recherche (ANR-10-IDEX-001-02)

  • Guilhem Doulcier
  • Paul B Rainey

Agence Nationale de la Recherche (ANR-10-LABX-54)

  • Silvia De Monte

Agence Nationale de la Recherche (ANR-11-IDEX-0001-02)

  • Silvia De Monte

Max-Planck-Gesellschaft

  • Paul B Rainey

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

Reviewing Editor

  1. Wenying Shou, Fred Hutchinson Cancer Research Center, United States

Version history

  1. Received: November 7, 2019
  2. Accepted: June 12, 2020
  3. Accepted Manuscript published: July 7, 2020 (version 1)
  4. Version of Record published: August 20, 2020 (version 2)

Copyright

© 2020, Doulcier 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

  • 3,070
    views
  • 488
    downloads
  • 48
    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. Guilhem Doulcier
  2. Amaury Lambert
  3. Silvia De Monte
  4. Paul B Rainey
(2020)
Eco-evolutionary dynamics of nested Darwinian populations and the emergence of community-level heredity
eLife 9:e53433.
https://doi.org/10.7554/eLife.53433

Share this article

https://doi.org/10.7554/eLife.53433

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.