Topological constraints in early multicellularity favor reproductive division of labor

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.

Data availability

All evolutionary simulations and other computations associated with this work are available at github.com/dyanni3/topologicalConstraintsSpecialization; all parameters used in the current study are specified so all simulations can be repeated exactly.

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.

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

  • 3,323
    views
  • 439
    downloads
  • 40
    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. David Yanni
  2. Shane Jacobeen
  3. Pedro Márquez-Zacarías
  4. Joshua S Weitz
  5. William C Ratcliff
  6. Peter J Yunker
(2020)
Topological constraints in early multicellularity favor reproductive division of labor
eLife 9:e54348.
https://doi.org/10.7554/eLife.54348

Share this article

https://doi.org/10.7554/eLife.54348

Further reading

    1. Evolutionary Biology
    Mattias Siljestam, Claus Rueffler
    Research Article Updated

    The majority of highly polymorphic genes are related to immune functions and with over 100 alleles within a population, genes of the major histocompatibility complex (MHC) are the most polymorphic loci in vertebrates. How such extraordinary polymorphism arose and is maintained is controversial. One possibility is heterozygote advantage (HA), which can in principle maintain any number of alleles, but biologically explicit models based on this mechanism have so far failed to reliably predict the coexistence of significantly more than 10 alleles. We here present an eco-evolutionary model showing that evolution can result in the emergence and maintenance of more than 100 alleles under HA if the following two assumptions are fulfilled: first, pathogens are lethal in the absence of an appropriate immune defence; second, the effect of pathogens depends on host condition, with hosts in poorer condition being affected more strongly. Thus, our results show that HA can be a more potent force in explaining the extraordinary polymorphism found at MHC loci than currently recognised.

    1. Ecology
    2. Evolutionary Biology
    Rebecca D Tarvin, Jeffrey L Coleman ... Richard W Fitch
    Research Article

    Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here, we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration — passive accumulation — that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics, we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins.