, 36:105

Optimisations and evolution of the mammalian respiratory system

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Abstract

The respiratory system of mammalians is made of two successive branched structures with different physiological functions. The upper structure, or bronchial tree, is a fluid transportation system made of approximately 15 generations of bifurcations leading to the order of about 215 = 30, 000 terminal bronchioles with a diameter of approximately 0.5mm in the human lung. The branching pattern continues up to generation 23 but the structure and function of each of the subsequent structures, called acini, is different. Each acinus consists in a branched system of ducts surrounded by alveoli and plays the role of a diffusion cell where oxygen and carbon dioxide are exchanged with blood across the alveolar membrane. We show here that the bronchial tree simultaneously presents several different optimal properties. It is first energy efficient, second, it is space filling and third it is also “rapid”. This physically based multi-optimality suggests that, in the course of evolution, an organ selected against one criterion could have been used later for a totally different purpose. For example, once selected for its energetic efficiency for the transport of a viscous fluid like blood, the same genetic material could have been used for its optimized rapidity. This would have allowed the emergence of atmospheric respiration made of inspiration-expiration cycles. For this phenomenon to exist, rapidity is essential as fresh air has to reach the gas exchange organs, the pulmonary acini, before the beginning of expiration. We finally show that the pulmonary acinus is optimized in the sense that the acinus morphology is directly related to the notion of a “best possible” extraction of entropic energy by a diffusion exchanger that has to feed oxygen efficiently from air to blood across a membrane of finite permeability.

Graphical abstract

Contribution to the Topical Issue “Physical constraints of morphogenesis and evolution”, edited by Vincent Fleury, Paul François and Marie Christine Ho Ba Tho.