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. 2017 Sep 13;284(1862):20171348.
doi: 10.1098/rspb.2017.1348.

Quantitative study of developmental biology confirms Dickinsonia as a metazoan

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Quantitative study of developmental biology confirms Dickinsonia as a metazoan

Renee S Hoekzema et al. Proc Biol Sci. .

Abstract

The late Ediacaran soft-bodied macroorganism Dickinsonia (age range approx. 560-550 Ma) has often been interpreted as an early animal, and is increasingly invoked in debate on the evolutionary assembly of eumetazoan body plans. However, conclusive positive evidence in support of such a phylogenetic affinity has not been forthcoming. Here we subject a collection of Dickinsonia specimens interpreted to represent multiple ontogenetic stages to a novel, quantitative method for studying growth and development in organisms with an iterative body plan. Our study demonstrates that Dickinsonia grew via pre-terminal 'deltoidal' insertion and inflation of constructional units, followed by a later inflation-dominated phase of growth. This growth model is contrary to the widely held assumption that Dickinsonia grew via terminal addition of units at the end of the organism bearing the smallest units. When considered alongside morphological and behavioural attributes, our developmental data phylogenetically constrain Dickinsonia to the Metazoa, specifically the Eumetazoa plus Placozoa total group. Our findings have implications for the use of Dickinsonia in developmental debates surrounding the metazoan acquisition of axis specification and metamerism.

Keywords: Ediacaran; bilaterian; development; metazoan evolution; ontogeny.

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Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
The terminology used herein to describe Dickinsonia costata, and various morphological features discussed in the text. Images are of specimens SAM P40135 (D14, centre) and SAM P49355 (D17, right). Unit count is the total number of units counted within a specimen. Unit number denotes the order in which units were added in an individual specimen, assuming growth from a specific generative zone. Scale bars, 10 mm. (Online version in colour.)
Figure 2.
Figure 2.
Measurements of Dickinsonia unit length plotted against unit number and unit count (see text for definitions), assuming traditionally envisaged AD-end insertion. The measurements from individual specimens plot as arcs of points at a fixed unit count, with the unit number counted consecutively from the D-end. Inset: frontal view of the same plot. Specimens within different groups plot on distinct growth surfaces, with D. rex and D. costata clearly displaying different growth trajectories.
Figure 3.
Figure 3.
Growth data for Dickinsonia specimens assuming (a) an anti-deltoidal (AD-end) and (b) a deltoidal (D-end) generative zone, plotted as (i) complete growth surfaces with units counted from the end interpreted as the oldest, (ii) growth lines of the lengths of individual units as a function of unit count for selected specimens, formed by connecting the measurements of units perceived to be homologous, and (iii) as plots of unit number against unit length, with each continuous line illustrating the measurements of a single specimen, and dotted lines connecting longest units of least and most contracted specimens. Legend for colour coding as in figure 2. The AD-end units of some specimens (particularly D15) could not be measured, so the number of missing units was estimated.
Figure 4.
Figure 4.
Translation of the growth surface for D. costata specimen data (from uncontracted specimens) to a modelled growth surface, which renders unit lengths as a function of unit number and model time. Insets illustrate the measured and modelled growth of an individual unit, analogous to the growth lines in figure 3b. Each unit slows its relative growth after it has become the longest unit. With the additional input of unit angles and widths, this information can be used to render a model morphology at each point in time (see the interactive applet). (Online version in colour.)

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