Evolution of Multicellular Complexity in the Dictyostelid Social Amoebas

Kin, Koryu; Schaap, Pauline

doi:10.20944/preprints202102.0300.v1

“…1C), while the homolog of regA in C. reinhardtii responds to environmental stresses, and induces a similar switch from a reproductive to a non-reproductive cellular phenotype (31). A similar scenario played out in the case of the facultatively multicellular dictyostid amoebas; the signaling molecules responsible for differentiation in multicellular species are instead produced in response to cold stress in unicellular dictyostelids (32).…”

Section: Elaboration Of Organisms Through Cell Type Inventionmentioning

confidence: 92%

“…Moreover, development is also plastic and trajectories leading to particular cell types can shift. For example, in the ancestral multicellular dictyostelids, stalk-cells likely differentiated from pre-spore cells, whereas in the more recent group-4 dictyostelids, stalk cells differentiate from the developmentally distinct pre-stalk cells (32). The potential for this plasticity can also be seen in our own cells, where expression of a single transcription factor, MYOD, can switch a fibroblast into a skeletal muscle cell (3).…”

Section: Cell Type Evolution Encoded In Gene Regulation and Reflected...mentioning

confidence: 99%

A topological look into the evolution of developmental programs

Mani¹,

Tlusty²

2021

Preprint

0

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Rapid advance of experimental techniques provides an unprecedented in-depth view into complex developmental processes. Still, little is known on how the complexity of multicellular organisms evolved by elaborating developmental programs and inventing new cell types. A hurdle to understanding developmental evolution is the difficulty of even describing the intertwined network of spatiotemporal processes underlying the development of complex multicellular organisms. Nonetheless, an overview of developmental trajectories can be obtained from cell type lineage maps. Here, we propose that these lineage maps can also reveal how developmental programs evolve: the modes of evolving new cell types in an organism should be visible in its developmental trajectories, and therefore in the geometry of its cell type lineage map. This idea is demonstrated using a parsimonious generative model of developmental programs, which allows us to reliably survey the universe of all possible programs and examine their topological features. We find that, contrary to belief, tree-like lineage maps are rare and lineage maps of complex multicellular organisms are likely to be directed acyclic graphs where multiple developmental routes can converge on the same cell type. While cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs which produce low-functioning organisms. Our model indicates that additionally, lineage map topologies are correlated with such a functional property: the ability of organisms to regenerate. SIGNIFICANCE Cell type invention is a chief process in the evolution of developmental programs. Traditionally, developmental trajectories are represented as cell type lineage maps. Here we propose that systematic analysis of these maps, in particular their topology, should reveal traces of the manner in which cell types were invented. This is illustrated using a generative model of developmental programs, which allows one to robustly survey the geometry of cell lineage maps and link them to modes of cell type invention. We suggest that predictions made by such mathematical models, in conjunction with surveys of real cell-lineage maps of different multicellular lineages could uncover mechanisms underlying evolution of developmental programs.

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“…1 C), whereas the homolog of regA in C. reinhardtii responds to environmental stresses and induces a similar switch from a reproductive to a nonreproductive cellular phenotype (31). A similar scenario played out in the case of the facultatively multicellular dictyostid amoebas; the signaling molecules responsible for differentiation in multicellular species are instead produced in response to cold stress in unicellular dictyostelids (32).…”

Section: Elaboration Of Organisms Through Cell Type Inventionmentioning

confidence: 94%

“…Moreover, development is also plastic, and trajectories leading to particular cell types can shift. For example, in the ancestral multicellular dictyostelids, stalk cells likely differentiated from prespore cells, whereas in the more recent group 4 dictyostelids, stalk cells differentiate from the developmentally distinct prestalk cells (32). The potential for this plasticity can also be seen in our own cells, in which expression of a single transcription factor, MYOD, can switch a fibroblast into a skeletal muscle cell (3).…”

Section: Cell Type Evolution Encoded In Gene Regulation and Reflected In Developmental Programsmentioning

confidence: 96%

A topological look into the evolution of developmental programs

Mani

¹

,

Tlusty

²

2021

Biophysical Journal

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Rapid advance of experimental techniques provides an unprecedented in-depth view into complex developmental processes. Still, little is known on how the complexity of multicellular organisms evolved by elaborating developmental programs and inventing new cell types. A hurdle to understanding developmental evolution is the difficulty of even describing the intertwined network of spatiotemporal processes underlying the development of complex multicellular organisms. Nonetheless, an overview of developmental trajectories can be obtained from cell type lineage maps. Here, we propose that these lineage maps can also reveal how developmental programs evolve: the modes of evolving new cell types in an organism should be visible in its developmental trajectories and therefore in the geometry of its cell type lineage map. This idea is demonstrated using a parsimonious generative model of developmental programs, which allows us to reliably survey the universe of all possible programs and examine their topological features. We find that, contrary to belief, tree-like lineage maps are rare, and lineage maps of complex multicellular organisms are likely to be directed acyclic graphs in which multiple developmental routes can converge on the same cell type. Although cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs that produce low-functioning organisms. Our model indicates that additionally, lineage map topologies are correlated with such a functional property: the ability of organisms to regenerate.

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“…Members of the slime mold clade Dictyostelia occupy a middle ground between single-celled and multicellular organisms (Kin and Schaap 2021;Schaap 2021). When food and moisture are abundant, they live and forage as unicellular organisms; when moisture evaporates or food becomes scarce, cells form cooperative aggregates ("slugs") and later a stalk capped by a fruiting body of spores ready to disperse.…”

Section: Fruiting Structures In the Slime Mold Dictyosteliummentioning

confidence: 99%

Co‐option of stress mechanisms in the origin of evolutionary novelties

Love

¹

,

Wagner

²

2022

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It is widely accepted that stressful conditions can facilitate evolutionary change. The mechanisms elucidated thus far accomplish this with a generic increase in heritable variation that facilitates more rapid adaptive evolution, often via plastic modifications of existing characters. Through scrutiny of different meanings of stress in biological research, and an explicit recognition that stressors must be characterized relative to their effect on capacities for maintaining functional integrity, we distinguish between: (1) previously identified stress‐responsive mechanisms that facilitate evolution by maintaining an adaptive fit with the environment, and (2) the co‐option of stress‐responsive mechanisms that are specific to stressors leading to the origin of novelties via compensation. Unlike standard accounts of gene co‐option that identify component sources of evolutionary change, our model documents the cost‐benefit trade‐offs and thereby explains how one mechanism—an immediate response to acute stress—is transformed evolutionarily into another—routine protection from recurring stressors. We illustrate our argument with examples from cell type origination as well as processes and structures at higher levels of organization. These examples suggest a general principle of evolutionary origination based on the capacity to switch between regulatory states related to reproduction and proliferation versus survival and differentiation.

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Evolution of Multicellular Complexity in the Dictyostelid Social Amoebas

Cited by 6 publications

References 105 publications

A topological look into the evolution of developmental programs

A topological look into the evolution of developmental programs

A topological look into the evolution of developmental programs

Co‐option of stress mechanisms in the origin of evolutionary novelties

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