1. Developmental Biology
  2. Evolutionary Biology

Evolution: Tracing the history of cell types

A study of sea urchin and sea star larvae paves the way for understanding how cell types evolve and give rise to novel morphologies.
https://doi.org/10.7554/eLife.90447
Share this article
Cite this article
  1. Antonia Grausgruber
  2. Roger Revilla-i-Domingo
(2023)
Evolution: Tracing the history of cell types
eLife 12:e90447.
https://doi.org/10.7554/eLife.90447
  2. Download BibTeX
  3. Download .RIS
  1. Antonia Grausgruber
  2. Roger Revilla-i-Domingo  Is a corresponding author
  1. Department of Neuroscience and Developmental Biology, University of Vienna, Austria
  2. Research Platform Single Cell Regulation of Stem Cells, University of Vienna, Austria
  3. Max Perutz Labs, University of Vienna, Austria

For decades scientists have been fascinated with how evolution gave rise to the wide range of shapes and sizes that exist in the animal kingdom today. At the heart of this morphological variation are the different cell types that make up an organism, some of which will be unique to certain species (Arendt et al., 2016). However, how new cell types emerged over the course of evolution is still hotly debated.

A group of animals known as echinoderms – which includes sea urchins, sea stars and brittle stars among others – offer a fascinating example of morphological novelty. Although their larvae share many morphological features, there are also some clear distinctions, making them a useful system for studying how specific cell types evolved. For instance, the two most well-studied echinoderms, sea stars and sea urchins, develop in a remarkably similar way. However, despite this, sea urchins have two cell types that are not found in sea stars (Figure 1A): skeletogenic mesenchyme cells, which make the mineral skeleton that gives sea urchin larvae their distinct shape, and pigmented cells that reside in the outer epithelium and are recruited to the immune system during an infection (Decker and Lennarz, 1988; Gustafson and Wolpert, 1967; Buckley and Rast, 2017). Now, in eLife, Veronica Hinman and colleagues from Carnegie Mellon University – including Anne Meyer as first author – report new insights in to how these two cell types emerged over the course of evolution (Meyer et al., 2023).

Figure 1
Download asset Open asset
Morphological novelties in the sea urchin larva.

(A) Schematic representation of the adult (top) and larval (bottom) forms of sea stars and sea urchins. Two larval cell types had been thought to be unique to the sea urchin: the skeletogenic mesenchyme cells that make the skeleton (red), and the pigment cells embedded in the larval epithelium (purple). Meyer et al. found that the skeletogenic mesenchyme cells express similar genes to the right coelomic pouch of the sea star larva (blue), and the pigment cells are similar to immune and neural cells of the sea star larva (not shown). (B) These cells were found to share regulatory mechanisms (represented by different coloured clockwork wheels). Pigment cells activate similar regulatory components as immune (orange wheel) and neural (yellow wheel) cells in sea stars. Unknown components (grey wheels) may control the interplay between the immune and neural functions of these cells. The right coelomic pouch of the sea star turns on regulatory components required to produce mesenchymal cells (green wheels) – epithelial to mesenchymal transition (EMT), cell migration, and tubulogenesis – which are also activated in skeletogenic mesenchyme cells in sea urchins. This suggests that skeletogenic mesenchyme cells and cells of the right coelomic pouch evolved from the same ancestor. Later in evolution, the skeletogenic mesenchyme cells acquired a skeletogenic program (red wheel), while the right coelomic pouch cells might have acquired other currently unknown programs (blue wheel).

Image credit: Antonia Grausgruber.

Cell types are typically defined based on their morphology, function, and where and when in the embryo they originated. But Meyer et al. propose that analysing these attributes alone is not sufficient for tracing how a cell type evolved. Instead, the team focused on the inner machinery that regulates all attributes of every cell. They did this by employing a technique called single-nuclei RNA sequencing, which reveals the genes expressed in every cell of an organism. This information can then be used to determine which cells activate similar regulatory mechanisms and therefore might be evolutionary related (Marioni and Arendt, 2017; Tanay and Sebé-Pedrós, 2021).

Meyer et al. used this powerful method to see how cells in the larva of a sea star compare to previously published sequencing data from the larva of a sea urchin (Foster et al., 2020). This revealed a very different picture than expected: both cell types that were thought to be unique to sea urchins appeared to have counterparts in the sea star larva (Figure 1A and B).

The skeletogenic mesenchyme cells of the developing sea urchin were similar to cells of the right coelomic pouch in the sea star which buds off the top of the embryonic structure that gives rise to the gut (Child, 1941). Many of the genes they shared are known to regulate the developmental processes required to generate mesenchymal cells, including epithelial to mesenchymal transition (EMT), cell migration and tubulogenesis. This suggests that skeletogenic mesenchyme cells and cells in the right coelomic pouch evolved from a common ancestor, which also possessed these regulatory mechanisms (Figure 1B). It is likely that these cells then evolutionarily diverged to activate the sets of genes responsible for building the skeleton in sea urchins (Gao and Davidson, 2008).

The pigment cells of the sea urchin were also found to be similar to immune and neural cell types in the sea star. Based on the genes shared between them, Meyer et al. propose that pigment cells have a dual role (immune and neural) in sea urchin larvae, while these functions are exerted by two separate cell types in sea stars (Figure 1B). Although a specific evolutionary history for these cell types is not provided in this study, these results support previous findings suggesting that immune and neural cells are evolutionarily related (Klimovich and Bosch, 2018).

A number of questions still remain about the evolutionary history of skeletogenic mesenchyme and pigment cells. For example, while the pigment cells seem to be unique to sea urchins, a larval skeleton is also present in other echinoderms, such as brittle stars. Extending the approach used by Meyer et al. to more echinoderms will provide a deeper understanding of how the cell types that give rise to the larval skeleton emerged. In addition, unravelling the networks of genes that control the development of skeletogenic mesenchyme and pigment cells in various echinoderms will help reveal the precise events that led to these evolutionary novelties. The findings of Meyer et al. provide a very fertile ground from which to address these questions, and more broadly how the enormous diversity of animal forms arose during evolution.

References

Article and author information

Author details

  1. Antonia Grausgruber

    Antonia Grausgruber is in the Department of Neuroscience and Developmental Biology, and the Research Platform Single Cell Regulation of Stem Cells, University of Vienna, Vienna, Austria
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0009-0005-9874-2882

  2. Roger Revilla-i-Domingo

    Roger Revilla-i-Domingo is in the Department of Neuroscience and Developmental Biology, and the Max Perutz Labs, University of Vienna, Vienna, Austria
    For correspondence
    roger.revilla-i-domingo@univie.ac.at
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7943-5776

Publication history

  1. Version of Record published:

Copyright

© 2023, Grausgruber and Revilla-i-Domingo

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,649
    views
  • 129
    downloads
  • 0
    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. Antonia Grausgruber
  2. Roger Revilla-i-Domingo
(2023)
Evolution: Tracing the history of cell types
eLife 12:e90447.
https://doi.org/10.7554/eLife.90447

Categories and tags

    1. Related to

    New hypotheses of cell type diversity and novelty from orthology-driven comparative single cell and nuclei transcriptomics in echinoderms

    Anne Meyer, Carolyn Ku ... Veronica Hinman
  2. Further reading

Further reading

    1. Developmental Biology
    2. Evolutionary Biology

    New hypotheses of cell type diversity and novelty from orthology-driven comparative single cell and nuclei transcriptomics in echinoderms

    Anne Meyer, Carolyn Ku ... Veronica Hinman
    Research Article Updated

    Cell types are the building blocks of metazoan biodiversity and offer a powerful perspective for inferring evolutionary phenomena. With the development of single-cell transcriptomic techniques, new definitions of cell types are emerging. This allows a conceptual reassessment of traditional definitions of novel cell types and their evolution. Research in echinoderms, particularly sea star and sea urchin embryos has contributed significantly to understanding the evolution of novel cell types, through the examination of skeletogenic mesenchyme and pigment cells, which are found in sea urchin larvae, but not sea star larvae. This paper outlines the development of a gene expression atlas for the bat sea star, Patiria miniata, using single nuclear RNA sequencing (snRNA-seq) of embryonic stages. The atlas revealed 23 cell clusters covering all expected cell types from the endoderm, mesoderm, and ectoderm germ layers. In particular, four distinct neural clusters, an immune-like cluster, and distinct right and left coelom clusters were revealed as distinct cell states. A comparison with Strongylocentrotus purpuratus embryo single-cell transcriptomes was performed using 1:1 orthologs to anchor and then compare gene expression patterns. The equivalent of S. purpuratus piwil3+ Cells were not detected in P. miniata, while the Left Coelom of P. miniata has no equivalent cell cluster in S. purpuratus. These differences may reflect changes in developmental timing between these species. While considered novel morphologically, the Pigment Cells of S. purpuratus map to clusters containing Immune-like Mesenchyme and Neural cells of P. miniata, while the Skeletogenic Mesenchyme of S. purpuratus are revealed as orthologous to the Right Coelom cluster of P. miniata. These results suggest a new interpretation of the evolution of these well-studied cell types and a reflection on the definition of novel cell types.

    1. Developmental Biology
    2. Neuroscience

    Embryonic origins of forebrain oligodendrocytes revisited by combinatorial genetic fate mapping

    Yuqi Cai, Zhirong Zhao ... Miao He
    Short Report

    Multiple embryonic origins give rise to forebrain oligodendrocytes (OLs), yet controversies and uncertainty exist regarding their differential contributions. We established intersectional and subtractional strategies to genetically fate map OLs produced by medial ganglionic eminence/preoptic area (MGE/POA), lateral/caudal ganglionic eminences (LGE/CGE), and dorsal pallium in the mouse brain. We found that, contrary to the canonical view, LGE/CGE-derived OLs make minimum contributions to the neocortex and corpus callosum, but dominate piriform cortex and anterior commissure. Additionally, MGE/POA-derived OLs, instead of being entirely eliminated, make small but sustained contribution to cortex with a distribution pattern distinctive from those derived from the dorsal origin. Our study provides a revised and more comprehensive view of cortical and white matter OL origins, and established valuable new tools and strategies for future OL studies.

    1. Developmental Biology
    2. Neuroscience

    Lateral/caudal ganglionic eminence makes limited contribution to cortical oligodendrocytes

    Jialin Li, Feihong Yang ... Zhuangzhi Zhang
    Short Report

    The emergence of myelinating oligodendrocytes represents a pivotal developmental milestone in vertebrates, given their capacity to ensheath axons and facilitate the swift conduction of action potentials. It is widely accepted that cortical oligodendrocyte progenitor cells (OPCs) arise from medial ganglionic eminence (MGE), lateral/caudal ganglionic eminence (LGE/CGE), and cortical radial glial cells (RGCs). Here, we used two different fate mapping strategies to challenge the established notion that the LGE generates cortical OPCs. Furthermore, we used a Cre/loxP-dependent exclusion strategy to reveal that the LGE/CGE does not give rise to cortical OPCs. Additionally, we showed that specifically eliminating MGE-derived OPCs leads to a significant reduction of cortical OPCs. Together, our findings indicate that the LGE does not generate cortical OPCs, contrary to previous beliefs. These findings provide a new view of the developmental origins of cortical OPCs and a valuable foundation for future research on both normal development and oligodendrocyte-related disease.