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The simplicity of metazoan cell lineages

Nature volume 433, pages 152–156 (2005)Cite this article

Abstract

Developmental processes are thought to be highly complex, but there have been few attempts to measure and compare such complexity across different groups of organisms1,2,3,4,5. Here we introduce a measure of biological complexity based on the similarity between developmental and computer programs6,7,8,9. We define the algorithmic complexity of a cell lineage as the length of the shortest description of the lineage based on its constituent sublineages9,10,11,12,13. We then use this measure to estimate the complexity of the embryonic lineages of four metazoan species from two different phyla. We find that these cell lineages are significantly simpler than would be expected by chance. Furthermore, evolutionary simulations show that the complexity of the embryonic lineages surveyed is near that of the simplest lineages evolvable, assuming strong developmental constraints on the spatial positions of cells and stabilizing selection on cell number. We propose that selection for decreased complexity has played a major role in moulding metazoan cell lineages.

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Figure 1: Example of the calculation of cell lineage complexity.
Figure 2: Metazoan embryonic cell lineages are simpler than expected by chance.
Figure 3: The simplicity of the ascidian cell lineage.
Figure 4: Metazoan cell lineages are not as simple as they could be.

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Acknowledgements

We thank S. Emmons, Y. Fofanov, D. Graur, D. Portman, T. Shin, S. Srinivasan and M. Travisano for discussions. Z. Altun and D. Hall gave advice on the classification of C. elegans cells. The Sun Microsystems Center of Excellence in the Geosciences at the University of Houston provided access to high-performance computing resources. The Foundation for Science and Technology (Portugal), European Molecular Biology Organization, Biotechnology and Biological Sciences Research Council (UK), and the University of Houston provided financial support.

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Authors and Affiliations

  1. Department of Biology and Biochemistry, University of Houston, Houston, Texas, 77204-5001, USA

    Ricardo B. R. Azevedo, Rolf Lohaus & Muralikrishna Umamaheshwar

  2. Division of Medical and Biological Informatics, German Cancer Research Center, Heidelberg, D-69120, Germany

    Rolf Lohaus, Volker Braun, Markus Gumbel, Ute Platzer & Hans-Peter Meinzer

  3. Department of Biology, Imperial College, Silwood Park, Ascot, SL5 7PY, UK

    Paul-Michael Agapow & Armand M. Leroi

  4. Department of Biology, Ghent University, Ghent, B-9000, Belgium

    Wouter Houthoofd & Gaëtan Borgonie

Authors
  1. Ricardo B. R. Azevedo
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Correspondence to Ricardo B. R. Azevedo.

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Supplementary information

Supplementary Movie

The spatial positions of cells in the Pellioditis marina embryo are largely determined by the cell lineage. The movie shows a simulation of the embryonic development of P. marina based on 4D microscopy data (Supplementary Methods). Development runs for approximately 530 minutes from shortly after the third cell division (4-cell stage) until the onset of muscle contraction (571-cell stage). Initially, the embryo is viewed from the ventral side, with anterior to the left, and then rotates to a left lateral position during elongation. Cells are coloured in a gradient from red to blue corresponding to their position in the lineage diagram from left to right (Supplementary Fig. S3). Cells undergoing programmed cell death turn white and become increasingly transparent before vanishing. (MOV 2568 kb)

Supplementary Methods

Details on cell lineage data, lineage complexity metric, and software. Additional references are included. (PDF 67 kb)

Supplementary Figures S1–6

Legends and references to accompany the below figures are also included in this file. Supplementary Fig. S1: our conclusions are robust to the way in which cells are classified. Supplementary Fig. S2: distributions of the effects of mutations on the complexity and lineage positions of cells for each of the metazoan lineages. Supplementary Fig. S3: the spatial positions of cells in the P. marina embryo are determined by the cell lineage. Supplementary Fig. S4: an extremely simple lineage capable of generating the terminal cells of the Caenorhabditis elegans embryo. Supplementary Fig. S5: the constraint on cell position is modeled as a selective constraint. Supplementary Fig. S6: the spatial constraint on the evolution of lineage complexity is not caused by an indirect reduction of population size. (PDF 155 kb)

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Azevedo, R., Lohaus, R., Braun, V. et al. The simplicity of metazoan cell lineages. Nature 433, 152–156 (2005). https://doi.org/10.1038/nature03178

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