Efficient vasculature investment in tissues can be determined without global information

Abstract

<jats:p>Cells are the fundamental building blocks of organs and tissues. Information and mass flow through cellular contacts in these structures is vital for the orchestration of organ function. Constraints imposed by packing and cell immobility limit intercellular communication, particularly as organs and organisms scale up to greater sizes. In order to transcend transport limitations, delivery systems including vascular and respiratory systems evolved to facilitate the movement of matter and information. The construction of these delivery systems has an associated cost, as vascular elements do not perform the metabolic functions of the organs they are part of. This study investigates a fundamental trade-off in vascularization in multicellular tissues: the reduction of path lengths for communication versus the cost associated with producing vasculature. Biologically realistic generative models, using multicellular templates of different dimensionalities, revealed a limited advantage to the vascularization of two-dimensional tissues. Strikingly, scale-free improvements in transport efficiency can be achieved even in the absence of global knowledge of tissue organization. A point of diminishing returns in the investment of additional vascular tissue to the increased reduction of path length in 2.5- and three-dimensional tissues was identified. Applying this theory to experimentally determined biological tissue structures, we show the possibility of a co-dependency between the method used to limit path length and the organization of cells it acts upon. These results provide insight as to why tissues are or are not vascularized in nature, the robustness of developmental generative mechanisms and the extent to which vasculature is advantageous in the support of organ function.</jats:p>

Embodiment in distributed information processing: “Solid” plants versus “liquid” ant colonies

“…Interestingly, the formation of these information transfer networks is themselves a result of developmental computations, giving rise to a ‘nested distributed computation’. As plant tissues grow, vascular systems develop to support efficient long range transport of water, nutrients and signalling molecules (Conn et al, 2017 ; Duran-Nebreda et al, 2020 ). However, since vascular cells do not contribute to primary organ function (e.g., photosynthesis in leaves and water and nutrient uptake in roots), they are also a costly investment (Conn et al, 2017 ; Duran-Nebreda et al, 2020 ).…”

“…As plant tissues grow, vascular systems develop to support efficient long range transport of water, nutrients and signalling molecules (Conn et al, 2017 ; Duran-Nebreda et al, 2020 ). However, since vascular cells do not contribute to primary organ function (e.g., photosynthesis in leaves and water and nutrient uptake in roots), they are also a costly investment (Conn et al, 2017 ; Duran-Nebreda et al, 2020 ). Nutrient travel time in tissues depends on both the fraction of vascular tissue and the organ dimensionality (flat or 2D, leaf-like or 2.5D, or fully 3D), and investments in vasculature were demonstrated to pay off only beyond 2D (Duran-Nebreda et al, 2020 ).…”

“…However, since vascular cells do not contribute to primary organ function (e.g., photosynthesis in leaves and water and nutrient uptake in roots), they are also a costly investment (Conn et al, 2017 ; Duran-Nebreda et al, 2020 ). Nutrient travel time in tissues depends on both the fraction of vascular tissue and the organ dimensionality (flat or 2D, leaf-like or 2.5D, or fully 3D), and investments in vasculature were demonstrated to pay off only beyond 2D (Duran-Nebreda et al, 2020 ). In their stems, plants lie along the Pareto front between total vascular branch length and nutrient transport distance, implying optimisation of this trade-off (Conn et al, 2017 ).…”

The Scaling of Blood Pressure and Volume

“…There was a renewed interest in the scaling of the cardiovascular system at the end of the 20th century due to a tentative explanation of the scaling of basal metabolic rate as related to blood supply in organisms [18]. That tentative explanation generated a prolific series of models, addressing in a general sense [19][20][21][22][23][24][25][26][27][28][29] the topology of supply networks from leaf venation and blood microvasculature to human transportation systems. However, none of these studies addressed the isometry of blood volume or the constancy of blood pressure.…”

“…Therefore, these two most relevant variables of a circulatory system, which are taken as roots for deriving the scaling rules of its other variables (see [19][20][21][22][23][24][25][26][27][28][29][30][31][32]), still remain without a theoretical basis to explain their own scaling.…”