1. Evolutionary Biology
Download icon

Topological constraints in early multicellularity favor reproductive division of labor

  1. David Yanni
  2. Shane Jacobeen  Is a corresponding author
  3. Pedro Márquez-Zacarías
  4. Joshua S Weitz
  5. William C Ratcliff  Is a corresponding author
  6. Peter J Yunker  Is a corresponding author
  1. Georgia Institute of Technology, United States
Research Article
  • Cited 0
  • Views 460
  • Annotations
Cite this article as: eLife 2020;9:e54348 doi: 10.7554/eLife.54348

Abstract

Reproductive division of labor (e.g., germ-soma specialization) is a hallmark of the evolution of multicellularity, signifying the emergence of a new type of individual and facilitating the evolution of increased organismal complexity. A large body of work from evolutionary biology, economics, and ecology has shown that specialization is beneficial when further division of labor produces an accelerating increase in absolute productivity (i.e., productivity is a convex function of specialization). Here we show that reproductive specialization is qualitatively different from classical models of resource sharing, and can evolve even when the benefits of specialization are saturating (i.e., productivity is a concave function of specialization). Through analytical theory and evolutionary individual-based simulations, we demonstrate that reproductive specialization is strongly favored in sparse networks of cellular interactions that reflect the morphology of early, simple multicellular organisms, highlighting the importance of restricted social interactions in the evolution of reproductive specialization.

Article and author information

Author details

  1. David Yanni

    School of Physics, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Shane Jacobeen

    School of Physics, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    shane.jacobeen@gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
  3. Pedro Márquez-Zacarías

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Joshua S Weitz

    School of Physics, Georgia Institute of Technology, Atlanta, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. William C Ratcliff

    School of Biological Sciences, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    william.ratcliff@gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. Peter J Yunker

    School of Physics, Georgia Institute of Technology, Atlanta, United States
    For correspondence
    peter.yunker@gatech.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8471-4171

Funding

National Science Foundation (IOS-1656549)

  • William C Ratcliff
  • Peter J Yunker

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

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Publication history

  1. Received: December 11, 2019
  2. Accepted: September 17, 2020
  3. Accepted Manuscript published: September 17, 2020 (version 1)

Copyright

© 2020, Yanni 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

  • 460
    Page views
  • 84
    Downloads
  • 0
    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)

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

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

Further reading

    1. Evolutionary Biology
    2. Genetics and Genomics
    Tom Hill, Robert L Unckless
    Research Article

    Hosts and viruses are constantly evolving in response to each other: as a host attempts to suppress a virus, the virus attempts to evade and suppress the host's immune system. Here we describe the recurrent evolution of a virulent strain of a DNA virus which infects multiple Drosophila species. Specifically, we identified two distinct viral types that differ 100-fold in viral titer in infected individuals, with similar differences observed in multiple species. Our analysis suggests that one of the viral types appears to have recurrently evolved at least 4 times in the past ~30,000 years, 3X in Arizona and once in another geographically distinct species. This recurrent evolution may be facilitated by an effective mutation rate which increases as each prior mutation increases viral titer and effective population size. The higher titer viral type suppresses the host immune system and an increased virulence compared to the low viral titer type.

    1. Evolutionary Biology
    2. Immunology and Inflammation
    Kazi Rahman et al.
    Research Article

    The interferon-inducible transmembrane (IFITM) proteins belong to the Dispanin/CD225 family and inhibit diverse virus infections. IFITM3 reduces membrane fusion between cells and virions through a poorly characterized mechanism. Mutation of proline rich transmembrane protein 2 (PRRT2), a regulator of neurotransmitter release, at glycine-305 was previously linked to paroxysmal neurological disorders in humans. Here, we show that glycine-305 and the homologous site in IFITM3, glycine-95, drive protein oligomerization from within a GxxxG motif. Mutation of glycine-95 (and to a lesser extent, glycine-91) disrupted IFITM3 oligomerization and reduced its antiviral activity against Influenza A virus. An oligomerization-defective variant was used to reveal that IFITM3 promotes membrane rigidity in a glycine-95-dependent and amphipathic helix-dependent manner. Furthermore, a compound which counteracts virus inhibition by IFITM3, amphotericin B, prevented the IFITM3-mediated rigidification of membranes. Overall, these data suggest that IFITM3 oligomers inhibit virus-cell fusion by promoting membrane rigidity.