The developmental biology of Charnia and the eumetazoan affinity of the Ediacaran rangeomorphs.

Frances S Dunn,Dmitriy V Grazhdankin,Simon Harris,Alexander G Liu,Emily Green,Philip Vixseboxse,Philip C J Donoghue,Joseph Flannery-Sutherland,Philip R Wilby

doi:10.1126/sciadv.abe0291

Abstract

Molecular timescales estimate that early animal lineages diverged tens of millions of years before their earliest unequivocal fossil evidence. The Ediacaran macrobiota (~574 to 538 million years ago) are largely eschewed from this debate, primarily due to their extreme phylogenetic uncertainty, but remain germane. We characterize the development of Charnia masoni and establish the affinity of rangeomorphs, among the oldest and most enigmatic components of the Ediacaran macrobiota. We provide the first direct evidence for the internal interconnected nature of rangeomorphs and show that Charnia was constructed of repeated branches that derived successively from pre-existing branches. We find homology and rationalize morphogenesis between disparate rangeomorph taxa, before producing a phylogenetic analysis, resolving Charnia as a stem-eumetazoan and expanding the anatomical disparity of that group to include a long-extinct bodyplan. These data bring competing records of early animal evolution into closer agreement, reformulating our understanding of the evolutionary emergence of animal bodyplans.

Highlights

Divergences between the early metazoan lineages are estimated by molecular clock analyses to have occurred tens of millions of years before the earliest unequivocal fossil records of their crown groups [1]
The frond of Charnia is composed of multiple levels of hierarchical branching, and previous descriptive ontological schemes for rangeomorphs describe these as first, second, third, and fourth-order branches, or primary, secondary, tertiary, and quaternary branches: terms that are applied to branches of the same scale across an individual frond [11, 12, 19]
Our 3D reconstruction of anatomy resolves Charnia as exhibiting successive branching orders that are derived from each other (Fig. 1, A to C): The entire width of the frond is filled with branching units, with no evidence for an axial stalk from which branches may differentiate

Summary

Introduction

Divergences between the early metazoan lineages are estimated by molecular clock analyses to have occurred tens of millions of years before the earliest unequivocal fossil records of their crown groups [1]. There is an emerging consensus that certain members of the Ediacaran macrobiota [~574 to 538 million years (Ma)], an infamously enigmatic group of fossilized macroscopic organisms whose affinities have long been contested, were early animals [4, 5] This general view is unsubstantiated for most taxa, and uncertainty over their phylogenetic affinities [e.g., [6]] means that these fossils have not contributed materially to debates surrounding metazoan divergence estimates. In large part, this uncertainty is a consequence of their unusual bodyplans, no better exemplified than by the frondose rangeomorphs. Patterns of morphogenesis remain untested in communities of taxa, with published hypotheses [15,16,17] derived from either isolated single characters or simulated data

Methods

Results

Conclusion