Modeling morphological diversity in the oldest large multicellular organisms

The terminal Neoproterozoic Ediacaran Period (635–541 Ma) is best described as a time of change. Following the end of the last global “Snowball” glaciation and a global rise in atmospheric oxygen levels, a biotic revolution began occurring in the oceans. The fossil record of this revolution showcases the transition from microscopic single cells into large, multicellular and morphologically complex organisms. Typifying this transition is the Ediacara biota, a group of globally distributed soft-bodied organisms whose affinities are fiercely debated and whose disappearance from the fossil record before the Cambrian explosion is equally perplexing (1, 2). Given the variation in shape, biological architecture, growth strategies, and body symmetries seen within the diverse Ediacara biota, it is most likely that these organisms represent an assortment of higher-level clades, many of which went extinct with the advent of bilaterian animals (2). Among the extinct clades, the Rangeomorpha (3) (Fig. 1) are particularly unusual in possessing repeating and apparently fractal branching architecture that is not known in any modern organisms (3). Rangeomorphs used a series of modular, millimeter-scale self-similar “frondlets” (Fig. 1, image 2) to construct a diverse array of larger, morphologically complex forms, including stalked fronds (Fig. 1, images 1–3), flat-lying mats (Fig. 1, image 4), lettuce-shaped bushes (Fig. 1, image 5), and erect fences (Fig. 1, image 6) (3). The remarkably high surface area-to-volume ratios generated as a result of this pseudofractal construction (4) suggest that these modules may represent the locus for passive diffusion-based (osmotrophic) (5) feeding, and could have aided oxygen uptake as well. Because of the uncertainty in their phylogenetic placement on the tree of life (6), many aspects of rangeomorph biology, including growth, development, reproductive strategies, and dispersal mechanisms remain elusive (although, see ref. 7). Now, innovative quantitative modeling of rangeomorph branching conducted by Cuthill and Conway Morris (8) is now shedding light on how these organisms came to dominate Ediacaran ecosystems.

Fig. 1.

Rangeomorph architecture. (1 and 2) Avalofractus with well-preserved modular frondlet. (3) Ediacaran frond Charnia. (4) Flat-lying mat-like Fractofusus. (5) Lettuce-shaped Bradgatia (ROM36500). (6) Fence-shaped Pectinifrons. (Scale bars: 1 cm in images 1–5; 1-cm increments in image 6.) Images 4, 5, and 6 courtesy of Dr. Guy M. Narbonne (Queen's University, Kingston, Ontario).

Cuthill and Conway Morris (8), through the use of a detailed quantitative parametric Lindenmayer-systems (L-systems) model, elegantly demonstrate the extent to which surface area influences the overall shape of Ediacaran rangeomorphs. Using just a limited number of morphological (mostly branching) parameters, the authors are able to model and digitally reproduce the known range of rangeomorph morphologies, highlighting the simplicity of their constructional parameters. Whether this will translate to simple genetic and developmental programs remains an interesting avenue of research. Furthermore, the authors demonstrate that the overwhelming majority of surface area (in most cases upwards of 95%) was provided directly by the fractal branching of the frond, even in forms characterized by sturdy stems and anchoring holdfasts (Fig. 1, image 1). This finding accentuates the importance of diffusion-based processes on the biological functioning of rangeomorphs, and highlights that diffusive nutrient acquisition was most likely the strongest competitive driver before the dominance of predatory behavior (2, 9, 10). Furthermore, Cuthill and Conway Morris show that rangeomorph shapes cluster into three dominant growth strategies, supporting previous suggestion of a three-tiered vertical stratification of Ediacaran deep-water ecosystems with a strong selective pressure for achieving greater height off the seafloor (11, 12). This selective pressure is exemplified by numerous different species attaining similar heights, despite favoring different growth and branching parameters. How to interpret the distinct tiering morphospace occupation is intriguing, as it could suggest that there are optimal tiering niches ideally suited for osmotrophy, or perhaps an ecologically driven constraint on rangeomorph morphology linked to osmotrpohic efficacy. Rangeomorphs directly competed for dissolved organic nutrients, which led to morphological and taxonomic diversification, subdivision of the immediate environment, and resulted in the earliest known example of macroscopic ecosystem construction and engineering (12). This finding stands in stark contrast to post-Ediacaran communities, where feeding is but one of many competitive drivers for diversification.

Another interesting outcome of the modeling by Cuthill and Conway Morris (8) may have significant implications on our understanding of rangeomorph evolutionary history. At present, there are no agreed-upon classification schemes for the overwhelming number of Ediacaran species, with most taxa occupying a “limbo-state” in terms of Linnaean hierarchical classification and overall evolutionary relationships (1, 2, 6). As for the Rangeomorpha, previous studies (e.g., ref. 3) highlighted the frondlet (Fig. 1, image 2) as the primary building block of rangeomorphs, and suggested that this unit may represent the single most-important unifying character for the group. However, Cuthill and Conway Morris (8) suggest that the frondlet is itself only part of a larger puzzle and that individual tubular units forming the modular frondlet may instead represent the underlying unifying character of the clade, as once proposed in the pioneering work of Seilacher (13). An underappreciated aspect of rangeomorph construction is that individual fondlets can vary in shape, number, and arrangement of tubular branches. These subtle differences in frondlet morphology have been interpreted as either biological or preservational (or in some cases both) (14, 15). As modeled by Cuthill and Conway Morris (8), each centimeter-scale frondlet is constructed by repeating, at multiple scales, a single tubular unit, which they suggest represents the single unifying characteristic of all rangeomorphs. If this is the case, it could explain the variation seen in overall frondlet construction among rangeomorph species, and perhaps elucidate the underlying evolutionary steps that resulted in the higher-order divisions within the rangeomorphs, most notably the distinction between the Rangida (Fig. 1, image 1) and Charnida (Fig. 1, image 3) (14, 15).

A powerful aspect of morphospace studies, such as those exemplified by Cuthill and Conway Morris (8), is the ability to quantitatively evaluate the efficacy of morphological constructions (16). The ability to measure the efficacy of diffusive processes can set realistic boundaries on their functional biology, which should aid immeasurably when it comes to understanding their phylogenetic affinities, and ultimately, their relationship (if any) to modern animals.