collaborateurs

Ebrahim Jahanbakhsh

Post-doctorant chez Évolution Naturelle & Artificielle

  • T: +41 22 379 31 22
  • office 4055a (Sciences III)

  • Self-organized patterning of crocodile head scales by compressive folding Nature 637, 375–383 (2025). https://doi.org/10.1038/s41586-024-08268-1

    résumé

    Amniote integumentary appendages constitute a diverse group of micro-organs, including feathers, hair and scales. These structures typically develop as genetically controlled units1, the spatial patterning of which emerges from a self-organized chemical Turing system2,3 with integrated mechanical feedback4,5. The seemingly purely mechanical patterning of polygonal crocodile head scales provides an exception to this paradigm6. However, the nature and origin of the mechanical stress field driving this patterning remain unclear. Here, using precise in ovo intravenous injections of epidermal growth factor protein, we generate Nile crocodile embryos with substantially convoluted head skin, as well as hatchlings with smaller polygonal head scales resembling those of caimans. We then use light-sheet fluorescence microscopy to quantify embryonic tissue-layer geometry, collagen architecture and the spatial distribution of proliferating cells. Using these data, we build a phenomenological three-dimensional mechanical growth model that recapitulates both normal and experimentally modified patterning of crocodile head scales. Our experiments and numerical simulations demonstrate that crocodile head scales self-organize through compressive folding, originating from near-homogeneous skin growth with differential stiffness of the dermis versus the epidermis. Our experiments and theoretical morphospace analyses indicate that variation in embryonic growth and material properties of skin layers provides a simple evolutionary mechanism that produces a diversity of head-scale patterns among crocodilian species.

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  • Mechanical positional information guides the self-organized development of a polygonal network of creases in the skin of mammalian noses. Curr Biol 2024 Oct;():. 10.1016/j.cub.2024.09.055. S0960-9822(24)01296-X.

    résumé

    The glabrous skin of the rhinarium (naked nose) of many mammalian species exhibits a polygonal pattern of grooves that retain physiological fluid, thereby keeping their nose wet and, among other effects, facilitating the collection of chemosensory molecules. Here, we perform volumetric imaging of whole-mount rhinaria from sequences of embryonic and juvenile cows, dogs, and ferrets. We demonstrate that rhinarial polygonal domains are not placode-derived skin appendages but arise through a self-organized mechanical process consisting of the constrained growth and buckling of the epidermal basal layer, followed by the formation of sharp epidermal creases exactly facing an underlying network of stiff blood vessels. Our numerical simulations show that the mechanical stress generated by excessive epidermal growth concentrates at the positions of vessels that form rigid base points, causing the epidermal layers to move outward and shape domes-akin to arches rising against stiff pillars. Remarkably, this gives rise to a larger length scale (the distance between the vessels) in the surface folding pattern than would otherwise occur in the absence of vessels. These results hint at a concept of "mechanical positional information" by which material properties of anatomical elements can impose local constraints on an otherwise globally self-organized mechanical pattern. In addition, our analyses of the rhinarial patterns in cow clones highlight a substantial level of stochasticity in the pre-pattern of vessels, while our numerical simulations also recapitulate the disruption of the folding pattern in cows affected by a hereditary disorder that causes hyperextensibility of the skin.

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  • The Unreasonable Effectiveness of Reaction Diffusion in Vertebrate Skin Color Patterning. Annu Rev Cell Dev Biol 2023 Oct;39():145-174. 10.1146/annurev-cellbio-120319-024414.

    résumé

    In 1952, Alan Turing published the reaction-diffusion (RD) mathematical framework, laying the foundations of morphogenesis as a self-organized process emerging from physicochemical first principles. Regrettably, this approach has been widely doubted in the field of developmental biology. First, we summarize Turing's line of thoughts to alleviate the misconception that RD is an artificial mathematical construct. Second, we discuss why phenomenological RD models are particularly effective for understanding skin color patterning at the meso/macroscopic scales, without the need to parameterize the profusion of variables at lower scales. More specifically, we discuss how RD models () recapitulate the diversity of actual skin patterns, () capture the underlying dynamics of cellular interactions, () interact with tissue size and shape, () can lead to ordered sequential patterning, () generate cellular automaton dynamics in lizards and snakes, () predict actual patterns beyond their statistical features, and () are robust to model variations. Third, we discuss the utility of linear stability analysis and perform numerical simulations to demonstrate how deterministic RD emerges from the underlying chaotic microscopic agents.

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  • Modeling convergent scale-by-scale skin color patterning in multiple species of lizards. Curr Biol 2022 Nov;():. S0960-9822(22)01692-X. 10.1016/j.cub.2022.10.044.

    résumé

    Skin color patterning in vertebrates emerges at the macroscale from microscopic cell-cell interactions among chromatophores. Taking advantage of the convergent scale-by-scale skin color patterning dynamics in five divergent species of lizards, we quantify the respective efficiencies of stochastic (Lenz-Ising and cellular automata, sCA) and deterministic reaction-diffusion (RD) models to predict individual patterns and their statistical attributes. First, we show that all models capture the underlying microscopic system well enough to predict, with similar efficiencies, neighborhood statistics of adult patterns. Second, we show that RD robustly generates, in all species, a substantial gain in scale-by-scale predictability of individual adult patterns without the need to parametrize the system down to its many cellular and molecular variables. Third, using 3D numerical simulations and Lyapunov spectrum analyses, we quantitatively demonstrate that, given the non-linearity of the dynamical system, uncertainties in color measurements at the juvenile stage and in skin geometry variation explain most, if not all, of the residual unpredictability of adult individual scale-by-scale patterns. We suggest that the efficiency of RD is due to its intrinsic ability to exploit mesoscopic information such as continuous scale colors and the relations among growth, scales geometries, and the pattern length scale. Our results indicate that convergent evolution of CA patterning dynamics, leading to dissimilar macroscopic patterns in different species, is facilitated by their spontaneous emergence under a large range of RD parameters, as long as a Turing instability occurs in a skin domain with periodic thickness. VIDEO ABSTRACT.

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