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Topological Phenotypes Constitute a New Dimension in the Phenotypic Space of Leaf Venation Networks

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  • Henrik Ronellenfitsch
  • Jana Lasser
  • Douglas C Daly
  • Eleni Katifori

Abstract

The leaves of angiosperms contain highly complex venation networks consisting of recursively nested, hierarchically organized loops. We describe a new phenotypic trait of reticulate vascular networks based on the topology of the nested loops. This phenotypic trait encodes information orthogonal to widely used geometric phenotypic traits, and thus constitutes a new dimension in the leaf venation phenotypic space. We apply our metric to a database of 186 leaves and leaflets representing 137 species, predominantly from the Burseraceae family, revealing diverse topological network traits even within this single family. We show that topological information significantly improves identification of leaves from fragments by calculating a “leaf venation fingerprint” from topology and geometry. Further, we present a phenomenological model suggesting that the topological traits can be explained by noise effects unique to specimen during development of each leaf which leave their imprint on the final network. This work opens the path to new quantitative identification techniques for leaves which go beyond simple geometric traits such as vein density and is directly applicable to other planar or sub-planar networks such as blood vessels in the brain.Author Summary: Planar reticular networks are ubiquitous in nature and engineering, formed for instance by the arterial vasculature in the mammalian neocortex, urban street grids or the vascular network of plant leaves. We use a topological metric to characterize the way loops are nested in such networks and analyze a large database of 186 leaves and leaflets, revealing for the first time that the nesting of the networks’ cycles constitutes a distinct phenotypic trait orthogonal to previously used geometric features. Furthermore, we demonstrate that the information contained in the leaf topology can significantly improve specimen identification from fragments, and provide an empirical growth model that can explain much of the observed data. Our work can improve understanding of the functional significance of the various leaf vein architectures and their correlation with the environment. It can pave the way for similar analyses in diverse areas of research involving reticulate networks.

Suggested Citation

  • Henrik Ronellenfitsch & Jana Lasser & Douglas C Daly & Eleni Katifori, 2015. "Topological Phenotypes Constitute a New Dimension in the Phenotypic Space of Leaf Venation Networks," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-12, December.
  • Handle: RePEc:plo:pcbi00:1004680
    DOI: 10.1371/journal.pcbi.1004680
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    References listed on IDEAS

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    1. Yuriy Mileyko & Herbert Edelsbrunner & Charles A Price & Joshua S Weitz, 2012. "Hierarchical Ordering of Reticular Networks," PLOS ONE, Public Library of Science, vol. 7(6), pages 1-9, June.
    2. Lawren Sack & Christine Scoffoni & Athena D. McKown & Kristen Frole & Michael Rawls & J. Christopher Havran & Huy Tran & Thusuong Tran, 2012. "Developmentally based scaling of leaf venation architecture explains global ecological patterns," Nature Communications, Nature, vol. 3(1), pages 1-10, January.
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    Cited by:

    1. Franz Kaiser & Philipp C. Böttcher & Henrik Ronellenfitsch & Vito Latora & Dirk Witthaut, 2022. "Dual communities in spatial networks," Nature Communications, Nature, vol. 13(1), pages 1-12, December.

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