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Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan

Significance Rangeomorph fronds characterize the late Ediacaran Period (575–541 Ma), representing some of the earliest large organisms. As such, they offer key insights into the early evolution of multicellular eukaryotes. However, their extraordinary branching morphology differs from all other organisms and has proved highly enigmatic. Here we provide a unified mathematical model of rangeomorph branching, allowing us to reconstruct 3D morphologies of 11 taxa and measure their functional properties. This reveals an adaptive radiation of fractal morphologies which maximized body surface area, consistent with diffusive nutrient uptake (osmotrophy). Rangeomorphs were adaptively optimal for the low-competition, high-nutrient conditions of Ediacaran oceans. With the Cambrian explosion in animal diversity (from 541 Ma), fundamental changes in ecological and geochemical conditions led to their extinction. The branching morphology of Ediacaran rangeomorph fronds has no exact counterpart in other complex macroorganisms. As such, these fossils pose major questions as to growth patterns, functional morphology, modes of feeding, and adaptive optimality. Here, using parametric Lindenmayer systems, a formal model of rangeomorph morphologies reveals a fractal body plan characterized by self-similar, axial, apical, alternate branching. Consequent morphological reconstruction for 11 taxa demonstrates an adaptive radiation based on 3D space-filling strategies. The fractal body plan of rangeomorphs is shown to maximize surface area, consistent with diffusive nutrient uptake from the water column (osmotrophy). The enigmas of rangeomorph morphology, evolution, and extinction are resolved by the realization that they were adaptively optimized for unique ecological and geochemical conditions in the late Proterozoic. Changes in ocean conditions associated with the Cambrian explosion sealed their fate.