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Modeling Morphological Diversity in the Oldest Large Multicellular COMMENTARY Modeling morphological diversity in the oldest large multicellular organisms Marc Laflamme1 including growth, development, reproduc- Department of Chemical and Physical Sciences, University of Toronto Mississauga, tive strategies, and dispersal mechanisms Mississauga, ON, Canada L5L 1C6 remain elusive (although, see ref. 7). Now, innovative quantitative modeling of ran- The terminal Neoproterozoic Ediacaran Pe- bilaterian animals (2). Among the extinct geomorph branching conducted by Cuthill riod (635–541 Ma) is best described as a time clades, the Rangeomorpha (3) (Fig. 1) are and Conway Morris (8) is now shedding of change. Following the end of the last global particularly unusual in possessing repeating light on how these organisms came to dom- “Snowball” glaciation and a global rise in at- and apparently fractal branching architecture inate Ediacaran ecosystems. mospheric oxygen levels, a biotic revolution that is not known in any modern organisms Cuthill and Conway Morris (8), through began occurring in the oceans. The fossil re- (3). Rangeomorphs used a series of modular, the use of a detailed quantitative parametric cord of this revolution showcases the transi- millimeter-scale self-similar “frondlets” (Fig. 1, Lindenmayer-systems (L-systems) model, el- tion from microscopic single cells into large, image 2) to construct a diverse array of larger, egantly demonstrate the extent to which sur- multicellular and morphologically complex morphologically complex forms, including face area influences the overall shape of organisms. Typifying this transition is the stalked fronds (Fig. 1, images 1–3), flat-lying Ediacaran rangeomorphs. Using just a limited Ediacara biota, a group of globally distributed mats (Fig. 1, image 4), lettuce-shaped bushes number of morphological (mostly branch- soft-bodied organisms whose affinities are (Fig. 1, image 5), and erect fences (Fig. 1, ing) parameters, the authors are able to fiercely debated and whose disappearance image 6) (3). The remarkably high surface model and digitally reproduce the known from the fossil record before the Cambrian area-to-volume ratios generated as a result range of rangeomorph morphologies, high- explosion is equally perplexing (1, 2). Given of this pseudofractal construction (4) suggest lighting the simplicity of their constructional the variation in shape, biological architecture, that these modules may represent the locus parameters. Whether this will translate to growth strategies, and body symmetries seen for passive diffusion-based (osmotrophic) (5) simple genetic and developmental programs within the diverse Ediacara biota, it is most feeding, and could have aided oxygen uptake remains an interesting avenue of research. likely that these organisms represent an as- as well. Because of the uncertainty in their Furthermore, the authors demonstrate that sortment of higher-level clades, many of phylogenetic placement on the tree of life the overwhelming majority of surface area which went extinct with the advent of (6), many aspects of rangeomorph biology, (in most cases upwards of 95%) was pro- vided 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 acquisi- tion was most likely the strongest competitive driver before the dominance of predatory be- havior(2,9,10).Furthermore,Cuthilland 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 se- lective 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 Author contributions: M.L. wrote the paper. Fig. 1. Rangeomorph architecture. (1 and 2) Avalofractus with well-preserved modular frondlet. (3) Ediacaran The author declares no conflict of interest. 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. See companion article on page 13122. Guy M. Narbonne (Queen’s University, Kingston, Ontario). 1Email: [email protected]. 12962–12963 | PNAS | September 9, 2014 | vol. 111 | no. 36 www.pnas.org/cgi/doi/10.1073/pnas.1412523111 Downloaded by guest on September 29, 2021 isintriguing,asitcouldsuggestthatthereare unifying character of the clade, as once pro- underlying evolutionary steps that resulted in COMMENTARY optimal tiering niches ideally suited for osmo- posed in the pioneering work of Seilacher the higher-order divisions within the rangeo- trophy, or perhaps an ecologically driven con- (13). An underappreciated aspect of rangeo- morphs, most notably the distinction between straint on rangeomorph morphology linked morph construction is that individual fondlets theRangida(Fig.1,image1)andCharnida to osmotrpohic efficacy. Rangeomorphs direct- can vary in shape, number, and arrangement (Fig. 1, image 3) (14, 15). ly competed for dissolved organic nutrients, of tubular branches. These subtle differences A powerful aspect of morphospace studies, which led to morphological and taxonomic in frondlet morphology have been interpreted such as those exemplified by Cuthill and diversification, subdivision of the immediate as either biological or preservational (or in Conway Morris (8), is the ability to quan- environment, and resulted in the earliest some cases both) (14, 15). As modeled by Cut- titatively evaluate the efficacy of morpho- known example of macroscopic ecosystem hill and Conway Morris (8), each centimeter- logical constructions (16). The ability to construction and engineering (12). This scale frondlet is constructed by repeating, at measure the efficacy of diffusive processes finding stands in stark contrast to post- multiple scales, a single tubular unit, which can set realistic boundaries on their func- Ediacaran communities, where feeding is they suggest represents the single unifying tional biology, which should aid immea- but one of many competitive drivers for characteristic of all rangeomorphs. If this is surably when it comes to understanding diversification. the case, it could explain the variation seen their phylogenetic affinities, and ulti- Another interesting outcome of the mod- in overall frondlet construction among ran- mately, their relationship (if any) to mod- elingbyCuthillandConwayMorris(8)may geomorph species, and perhaps elucidate the ern animals. have significant implications on our under- standing of rangeomorph evolutionary his- tory. At present, there are no agreed-upon 1 Erwin DH, et al. (2011) The Cambrian conundrum: Early 8 Cuthill JFH, Conway Morris S (2014) Fractal branching divergence and later ecological success in the early history of animals. organizations of Ediacaran rangeomorph fronds reveal a lost classification schemes for the overwhelming Science 334(6059):1091–1097. Proterozoic body plan. Proc Natl Acad Sci USA 111:13122–13126. number of Ediacaran species, with most taxa 2 Laflamme M, Darroch SAF, Tweedt SM, Peterson KJ, Erwin DH 9 Seilacher A, Grazhdankin D, Legouta A (2003) Ediacaran biota: The “ ” (2013) The end of the Ediacara biota: Extinction, biotic replacement, dawn of animal life in the shadow of giant protists. Paleontological occupying a limbo-state in terms of Lin- or Cheshire Cat? Gond Res 23(2):558–573. Research 7(1):43–54. naean hierarchical classification and overall 3 Narbonne GM (2004) Modular construction of early Ediacaran 10 Marshall CR (2006) Explaining the Cambrian “explosion” of evolutionary relationships (1, 2, 6). As for complex life forms. Science 305(5687):1141–1144. animals. Annu Rev Earth Planet Sci 34():355–384. 4 Laflamme M, Xiao S, Kowalewski M (2009) From the cover: 11 Clapham ME, Narbonne GM (2002) Ediacaran epifaunal tiering. the Rangeomorpha, previous studies (e.g., Osmotrophy in modular Ediacara organisms. Proc Natl Acad Sci USA Geology 30(7):627–630. ref. 3) highlighted the frondlet (Fig. 1, image 106(34):14438–14443. 12 Ghisalberti M, et al. (2014) Canopy flow analysis reveals the 2) as the primary building block of rangeo- 5 Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and advantage of size in the oldest communities of multicellular its implications for Precambrian palaeobiology. The Rise and Fall of eukaryotes. Curr Biol 24(3):305–309. morphs, and suggested that this unit may the Ediacaran Biota. eds Vickers-Rich P, Komarower P, Geol Soc Lon 13 Seilacher A (1989) Vendozoa: Organismic construction in the represent the single most-important unifying Spec Pub 286:355–368. Proterozoic biosphere. Lethaia 22(3):229–239. 6 Xiao S, Laflamme M (2009) On the eve of animal radiation: 14 Narbonne GM, Laflamme M, Greentree C, Trusler P (2009) character for the group. However, Cuthill and Phylogeny, ecology and evolution of the Ediacara biota. Trends Ecol Reconstructing a lost world: Ediacaran rangeomorphs from Conway Morris (8) suggest that the frondlet Evol 24(1):31–40. Spaniard’s Bay, Newfoundland. J Paleo 83(4):503–523. is itself only part of a larger puzzle and that 7 Darroch SAF, Laflamme M, Clapham ME (2013) Population 15 Brasier MD, Antcliffe JB, Liu AG (2012) The architecture of structure of the oldest known macroscopic communities Ediacaran fronds. Palaeontology 55(5):1105–1124. individual tubular units forming the modular from Mistaken Point, Newfoundland. Paleobiology 39(7): 16 Niklas KJ (1999) Evolutionary walks through a land plant frondlet may instead represent the underlying 591–604. morphospace. J Exp Bot 50(330):39–52. Laflamme PNAS | September 9, 2014 | vol. 111 | no. 36 | 12963 Downloaded by guest on September 29, 2021.
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