Ediacaran developmental biology

Abstract

Rocks of the Ediacaran System (635-541 Ma) preserve fossil evidence of some of the earliest complex macroscopic organisms, many of which have been interpreted as animals. However, the unusual morphologies of some of these organisms have made it difficult to resolve their biological relationships to modern metazoan groups. Alternative competing phylogenetic interpretations have been proposed for Ediacaran taxa, including algae, fungi, lichens, rhizoid protists, and even an extinct higher-order group (Vendobionta). If a metazoan affinity can be demonstrated for these organisms, as advocated by many researchers, they could prove informative in debates concerning the evolution of the metazoan body axis, the making and breaking of axial symmetries, and the appearance of a metameric body plan. Attempts to decipher members of the enigmatic Ediacaran macrobiota have largely involved study of morphology: comparative analysis of their developmental phases has received little attention. Here we present what is known of ontogeny across the three iconic Ediacaran taxa Charnia masoni, Dickinsonia costata and Pteridinium simplex, together with new ontogenetic data and insights. We use these data and interpretations to re-evaluate the phylogenetic position of the broader Ediacaran morphogroups to which these taxa are considered to belong (rangeomorphs, dickinsoniomorphs and erniettomorphs). We conclude, based on the available evidence, that the affinities of the rangeomorphs and the dickinsoniomorphs lie within Metazoa.

Keywords: Bilateria; Ediacaran; Eumetazoa; Metazoa; development; evolution.

Figure 1

Ediacaran rangeomorph taxa. (A) Beothukis plumosa, Newfoundland, Canada. (B) Fractofusus andersoni, Newfoundland, Canada. (C) Pectinifrons abyssalis, Newfoundland, Canada. (D) Bradgatia sp., Newfoundland, Canada. (E) Charnia masoni, UK. (F) Higher‐order branching in an exceptionally preserved Bradgatia sp. specimen from Newfoundland. (G) Stylised interpretation of growth of primary branches in Charnia masoni. (H) The different orders of rangeomorph branches, and their arrangement within Charnia masoni: 1 = primary branch, 2 = secondary branch, 3 = tertiary branch and 4 = quaternary branch. Grey overlay in A–E indicates a primary branch. Scale bars: A, B, D and E = 10 mm, C = 5 cm.

Figure 2

The length of Charnia masoni specimens plotted against the number of primary branches in specimens from: (A) Sword Point, Newfoundland, Canada (data from Laflamme et al., 2007) (data have been retrodeformed); (B) North Quarry Bed B, Charnwood Forest, Leicestershire, UK (data from Wilby et al., 2015) (data were not retrodeformed). Linear models represented by solid line (fitted through a subset of data in B – excluding the two largest specimens); broken line represents a second‐order polynomial model. Both populations show a linear relationship between specimen size and the number of primary branches up to specimens 49 cm in length [P = 0.003429 and P = 5.327 × 10⁻¹¹ for the Laflamme et al. (2007) and Wilby et al. (2015) data sets, respectively]; specimens larger than this are not explained by a linear model [the complete Wilby et al. (2015) data set is best fitted by a second‐order polynomial model, P = 1.579 × 10⁻¹⁰].

Figure 3

The development of the ‘stem’ region in Charnia masoni. (A, B) Charnia masoni from Pigeon Cove, Mistaken Point Ecological Reserve, Newfoundland, Canada (A) and outline of specimen (B). (C) Charnia masoni from Charnwood Forest, Leicestershire, UK. (D, E) Stem area (enlargement of boxed region in C) (D), and in outline (E). Illustrations to second‐order branch sub‐division. Scale bars: A = 5 mm, C = 5 cm, D = 10 mm.

Figure 4

Ediacaran dickinsoniomorph taxa. (A) Andiva ivantsovi, White Sea, Russia. [Palaeontological Institute Moscow (PIN) specimen number 3993–5623]. (B, C) Enlargements of the boxed area in A. The areas of unit differentiation are indicated by white arrows, and undivided regions on Andiva and Yorgia are indicated by black arrows. (D) Dickinsonia costata, South Australia [South Australia Museum (SAM) specimen numbers P49354 and P49355]. (E) Yorgia waggoneri, White Sea, Russia (Holotype PIN 3993–5024). (F) Stylised interpretation of growth of Dickinsonia costata, following the growth model proposed in Hoekzema et al. (2017). Scale bars = 10 mm.

Figure 5

Ediacaran erniettomorph taxa. (A, B) Pteridinium simplex, Namibia. Numbers identifying the three identified vanes. (C) Swartpuntia germsii, Namibia. (D) Ernietta plateauensis, Namibia. Scale bars = 10 mm. Images courtesy of D. Grazhdankin (A and B from Grazhdankin & Seilacher, 2002), M.D. Brasier (C), and M. Laflamme (D).

Figure 6

Schematic diagram showing the forms of growth observed in extant clades with serial repetition of component units; red indicates the style/feature of growth discussed. (A) Coordinated modular growth, seen in certain metazoan groups. (B) Parallel modular growth, common in plants and red, green and brown algae, with an aberrant branch highlighted in red. (C, D) Positioning of different central (additional growth zone highlighted with black arrow) and lateral growth zones/tips in extant serially repetitive groups. Single apical axes are seen in green and red algal groups, whereas multiple axes are seen in various metazoan and brown‐algal groups. (E) Diffuse growth, as seen in colonial bilaterian groups characterised by colony‐wide tip growth.

Figure 7

(A) Interpretive growth models of: 1, Charnia masoni; 2, Dickinsonia costata; 3, Andiva ivantsovi; 4, an extant bilaterian comparator. (B) A simplified eukaryote phylogeny including only groups with serially repetitive body plans to which the Ediacaran morphogroups have been compared. SAR = Stramenopiles, Alveolates and Rhizaria. The suggested phylogenetic positions of Charnia, Dickinsonia and Andiva are presented as discussed in the text (we include Andiva as possibly being resolved within the Bilateria because although our morphological data may suggest a truly terminal generative zone, this is based on one specimen and additional data are required to confirm or refute this). Green represents metazoan lineages. Dashed lines indicate the possible position of a group (owing to uncertainty surrounding the phylogeny of the basal Metazoa; e.g. Dunn et al., 2014).