Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Open Access

Computational topology of Drosophila melanogaster embryos: Emergent anatomy from the spatiotemporal distributions of hemocytes

Xinrui Hu1, Nickolay Korabel2, Tom H. Millard3,*, and Thomas Andrew Waigh1,†

  • 1Biological Physics Group, School of Physics and Astronomy, The University of Manchester, Oxford Rd., Manchester M13 9PL, United Kingdom
  • 2Department of Mathematics, The University of Manchester, Manchester M13 9PL, United Kingdom
  • 3Division of Developmental Biology and Medicine, Faculty of Biology, Medicine and Health, Oxford Rd., Manchester M13 9PL, United Kingdom

  • *Contact author: tom.millard@manchester.ac.uk
  • †Contact author: t.a.waigh@manchester.ac.uk

Phys. Rev. E 112, 044407 – Published 16 October, 2025

DOI: https://doi.org/10.1103/mc9z-kw1q

Abstract

Hemocytes migrate within Drosophila melanogaster embryos during their morphogenesis. The spatial distribution of the hemocytes reflects the emergent anatomy of the embryos. It poses a significant challenge to statistical characterization using conventional methods, such as mean-square displacements of tracks and Ripley's L function. This challenge arises from the complex heterogeneity of hemocyte dynamics and the variability of the organism's anatomy due to inherent nonlinear stochastic processes. We apply topological data analysis (TDA) to three different genotypes of Drosophila embryos: wild type, LanB1Df (extracellular matrix mutants), and SCARΔ37 (motility mutants). Computationally efficient methods are developed to characterize the embryos' topologies. Based on the Wasserstein distances, the LanB1 mutant is topologically distinct from the wild type and SCAR mutant, which are indistinguishable. Furthermore, an increase in the Betti-1 number (the number of holes in the hemocyte configurations) is observed across all samples with age, which is consistent with prior findings on cellular tiling behavior due to contact inhibition of locomotion. We also apply TDA methods to the hemocyte tracks within the embryos, allowing the wild type and SCAR mutant to be distinguished. Computational topology thus provides a robust method to quantify the emergent anatomy of embryos that is well suited to the complex heterogeneous datasets observed with hemocyte dynamics.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (39)

  1. G. Forgacs and S. A. Newman, Biological Physics of the Developing Embryo (Cambridge University Press, Cambridge, 2005).
  2. S. H. Holmes and W. Huber, Modern Statistics for Modern Biology (Cambridge University Press, Cambridge, 2018).
  3. N. Korabel, G. D. Clemente, D. Han, F. Feldman, T. H. Millard, and T. A. Waigh, Commun. Phys. 5, 269 (2022).
  4. D. Han, N. Korabel, R. Chen, M. Johnston, A. Gavrilova, V. J. Allan, S. Fedotov, and T. A. Waigh, eLife 9, e52224 (2020).
  5. T. A. Waigh and N. Korabel, Rep. Prog. Phys. 86, 126601 (2023).
  6. M. H. Baron, Developmental Hematopoiesis: Methods and Protocols (Humana, Totowa, 2005).
  7. M. Lavine and M. Strand, Insect Biochem. Mol. Biol. 32, 1295 (2002).
  8. R. Horwitz and D. Webb, Curr. Biol. 13, R756 (2003).
  9. A. Holz, B. Bossinger, T. Strasser, W. Janning, and R. Klapper, Development 130, 4955 (2003).
  10. W. Wood and A. Jacinto, Nat. Rev. Mol. Cell Biol. 8, 542 (2007).
  11. C. J. Hughes and J. R. Jacobs, Vet. Sci. 4, 24 (2017).
  12. L. I. Fessler, R. E. Nelson, and J. H. Fessler, Drosophila extracellular matrix, in Methods in Enzymology, edited by E. Ruoslahti and E. Engvall (Elsevier, Amsterdam, 1994), Vol. 245, pp. 271–294.
  13. B. Stramer, W. Wood, M. J. Galko, M. J. Redd, A. Jacinto, S. M. Parkhurst, and P. Martin, J. Cell Biol. 168, 567 (2005).
  14. A. Hohl, M. Zheng, W. Tang, E. Delmelle, and I. Casas, Spatiotemporal point pattern analysis using Ripley's K function, in Geospatial Data Science Techniques and Applications (CRC Press, Boca Raton, FL, 2017), pp. 155–176.
  15. X. Wang, F. Sohel, M. Bennamoun, Y. Guo, and H. Lei, Pattern Recog. 71, 414 (2017).
  16. A. M. Ibekwe, J. Ma, D. E. Crowley, C.-H. Yang, A. M. Johnson, T. C. Petrossian, and P. Y. Lum, Front. Cell. Infect. Microbiol. 4, 122 (2014).
  17. D. Bhaskar, W. Y. Zhang, A. Volkening, B. Sandstede, and I. Y. Wong, npj Syst. Biol. Appl. 9, 43 (2023).
  18. D. DeWoskin, J. Climent, I. Cruz-White, M. Vazquez, C. Park, and J. Arsuaga, Topol. Appl. 157, 157 (2010).
  19. E. J. Amézquita, M. Y. Quigley, T. Ophelders, E. Munch, and D. H. Chitwood, Dev. Dyn. 249, 816 (2020).
  20. D. Bhaskar, W. Y. Zhang, and I. Y. Wong, Soft Matter 17, 4653 (2021).
  21. N. Sepúlveda, L. Petitjean, O. Cochet, E. Grasland-Mongrain, P. Silberzan, and V. Hakim, PLoS Comput. Biol. 9, e1002944 (2013).
  22. N. Gal, D. Lechtman-Goldstein, and D. Weihs, Rheol. Acta 52, 425 (2013).
  23. A. Fuliński, J. Phys. A: Math. Theor. 50, 054002 (2017).
  24. D. A. Kenwright, A. W. Harrison, T. A. Waigh, P. G. Woodman, and V. J. Allan, Phys. Rev. E 86, 031910 (2012).
  25. L. L. Bonilla, A. Carpio, and C. Trenado, PLoS Comput. Biol. 16, e1008407 (2020).
  26. K. C. Nguyen, C. D. Jameson, S. A. Baldwin, J. T. Nardini, R. C. Smith, J. M. Haugh, and K. B. Flores, Math. Biosci. 370, 109158 (2024).
  27. J. Huisken and D. Y. R. Stainier, Development 136, 1963 (2009).
  28. B. J. Sáanchez-Sánchez, J. M. Urbano, K. Comber, A. Dragu, W. Wood, B. Stramer, and M. D. Martín-Bermudo, Cell Rep. 21, 1461 (2017).
  29. I. Evans, P. Ghai, V. Urbančič, K. L. Tan, and W. Wood, Cell Death Diff. 20, 709 (2013).
  30. F. Pedregosa, G. Varoquaux, A. Gramfort, V. Michel, B. Thirion, O. Grisel, M. Blondel, P. Prettenhofer, R. Weiss, V. Dubourg et al., J. Mach. Learn. Res. 12, 2825 (2011).
  31. M. Catanzaro, C. Tralie, and N. Saul, Persim—A scikit-tda project (Zenodo, Geneva, 2024), http://doi.org/10.5281/zenodo.2533369.
  32. X. Hu (GitHub, San Francisco, 2025), https://github.com/Ramarujun/Topological-Data-Analysis-of-Hemocytes.
  33. N. Otter, M. A. Porter, U. Tillmann, P. Grindrod, and H. A. Harrington, EPJ Data Sci. 6, 17 (2017).
  34. R. Ghrist, Bull. Am. Math. Soc. 45, 61 (2008).
  35. D. Cohen-Steiner, H. Edelsbrunner, J. Harer, and Y. Mileyko, Found. Comput. Math. 10, 127 (2010).
  36. J. R. Davis, C. Y. Huang, J. Zanet, S. Harrison, E. Rosten, S. Cox, D. Y. Soong, G. A. Dunn, and B. M. Stramer, Development 139, 4555 (2012).
  37. See Supplemental Material at http://link.aps.org/supplemental/10.1103/mc9z-kw1q for the distribution of track lengths for control, LanB1, and SCAR samples; analysis of Ripley's K functions to complement the Ripley L results in the main text; snapshots of hemocyte migration in Drosophila embryos; the effect of different persistence thresholds on Betti-1 calculations; and calculation of error bars for persistence diagrams.
  38. J. R. Davis, A. Luchici, F. Mosis, J. Thackery, J. A. Salazar, Y. Mao, G. A. Dunn, T. Betz, M. Miodownik, and B. M. Stramer, Cell 161, 361 (2015).
  39. T. A. Waigh, The Physics of Bacteria (Cambridge University Press, Cambridge, 2024).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation